Orai-STIM-mediated Ca2+ release from secretory granules revealed by a targeted Ca2+ and pH probe

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 51, 2012, Pages

  Dickson, Eamonn J ^a   Duman, Joseph G ^a,c   Moody, Mark W ^a   Chen, Liangyi ^b   Hille, Bertil ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b PEKING UNIVERSITY   (China)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Cameleon; FRET; IP3; Purinergic; SERCA

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM; CALCIUM CHANNEL; ORAI1 CHANNEL; PURINERGIC P2Y RECEPTOR; STROMAL INTERACTION MOLECULE 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CELL MEMBRANE; CHANNEL GATING; CULTURE MEDIUM; CYTOPLASM; ENDOPLASMIC RETICULUM; EXOCYTOSIS; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE CONSTRUCT; GENE OVEREXPRESSION; NONHUMAN; PH MEASUREMENT; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; RAT; RECEPTOR UPREGULATION; SECRETORY GRANULE; STORE OPERATED CALCIUM ENTRY;

CALCIUM; CALCIUM CHANNELS; CALCIUM SIGNALING; CELL LINE, TUMOR; CELL MEMBRANE; CYTOPLASM; ENDOPLASMIC RETICULUM; EXOCYTOSIS; HUMANS; HYDROGEN-ION CONCENTRATION; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; NEOPLASM PROTEINS; PHOTOCHEMISTRY; SECRETORY VESICLES;

EID: 84871386918     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1218247109     Document Type: Article

References (49)

1. Macrez N, Mironneau J (2004) Local Ca2+ signals in cellular signalling. Curr Mol Med 4(3):263-275.
2. Wu MM, et al. (2001) Mechanisms of pH regulation in the regulated secretory pathway. J Biol Chem 276(35):33027-33035.
3. Dittie AS, Hajibagheri N, Tooze SA (1996) The AP-1 adaptor complex binds to immature secretory granules from PC12 cells, and is regulated by ADP-ribosylation factor. J Cell Biol 132(4):523-536.
4. Verdugo P (1990) Goblet cells secretion and mucogenesis. Annu Rev Physiol 52:157-176.
5. Holroyd P, Lang T, Wenzel D, De Camilli P, Jahn R (2002) Imaging direct, dynamin-dependent recapture of fusing secretory granules on plasma membrane lawns from PC12 cells. Proc Natl Acad Sci USA 99(26):16806-16811.
6. Perrais D, Kleppe IC, Taraska JW, Almers W (2004) Recapture after exocytosis causes differential retention of protein in granules of bovine chromaffin cells. J Physiol 560(Pt 2):413-428.
7. Taraska JW, Perrais D, Ohara-Imaizumi M, Nagamatsu S, Almers W (2003) Secretory granules are recaptured largely intact after stimulated exocytosis in cultured endocrine cells. Proc Natl Acad Sci USA 100(4):2070-2075.
8. Hutton JC, Penn EJ, Peshavaria M (1983) Low-molecular-weight constituents of isolated insulin-secretory granules. Bivalent cations, adenine nucleotides and inorganic phosphate. Biochem J 210(2):297-305.
9. Winkler H, Westhead E (1980) The molecular organization of adrenal chromaffin granules. Neuroscience 5(11):1803-1823.
10. 2+ signals that are excluded from the nuclear region in pancreatic acinar cells. Pflugers Arch 432(6):1055-1061.
11. 2+) store in neuroendocrine cells with a vesicle-associated membrane protein aequorin chimaera. J Cell Biol 155(1):41-51.
12. Moreno A, et al. (2005) Calcium dynamics in catecholamine-containing secretory vesicles. Cell Calcium 37(6):555-564.
13. 2+. Nature 395(6705):908-912.
14. 2+ dynamics in the secretory vesicles of neurosecretory PC12 and INS1 cells. Cell Mol Neurobiol 30(8):1267-1274.
15. Blondel O, Bell GI, Seino S (1995) Inositol 1,4,5-trisphosphate receptors, secretory granules and secretion in endocrine and neuroendocrine cells. Trends Neurosci 18(4):157-161.
16. Mitchell KJ, Lai FA, Rutter GA (2003) Ryanodine receptor type I and nicotinic acid adenine dinucleotide phosphate receptors mediate Ca2+ release from insulin-containing vesicles in living pancreatic beta-cells (MIN6). J Biol Chem 278(13):11057-11064.
17. Putney JW, Jr. (1986) A model for receptor-regulated calcium entry. Cell Calcium 7(1):1-12.
18. 2+) entry. Nat Cell Biol 11(6):669-677.
19. Hogan PG, Lewis RS, Rao A (2010) Molecular basis of calcium signaling in lymphocytes: STIM and ORAI. Annu Rev Immunol 28:491-533.
20. Prakriya M, et al. (2006) Orai1 is an essential pore subunit of the CRAC channel. Nature 443(7108):230-233.
21. Zweifach A, Lewis RS (1995) Rapid inactivation of depletion-activated calcium current (ICRAC) due to local calcium feedback. J Gen Physiol 105(2):209-226.
22. 2+ overload. J Cell Sci 121(Pt 19):3133-3139.
23. 2+ entry. J Biol Chem 286(42):36448-36459.
24. 2+ analyzed with an improved genetically encoded fluorescent sensor. Proc Natl Acad Sci USA 101(50):17404-17409.
25. Heikal AA, Hess ST, Baird GS, Tsien RY, Webb WW (2000) Molecular spectroscopy and dynamics of intrinsically fluorescent proteins: coral red (dsRed) and yellow (Citrine). Proc Natl Acad Sci USA 97(22):11996-12001.
26. Wuytack F, Raeymaekers L, Missiaen L (2002) Molecular physiology of the SERCA and SPCA pumps. Cell Calcium 32(5-6):279-305.
27. Duman JG, Chen L, Hille B (2008) Calcium transport mechanisms of PC12 cells. J Gen Physiol 131(4):307-323.
28. Suh BC, Lee CO, Kim KT (1995) Signal flows from two phospholipase C-linked receptors are independent in PC12 cells. J Neurochem 64(3):1071-1079.
29. 2+ channels and T-lymphocyte activation by the pyrazole derivative BTP2. J Biol Chem 279(13):12427-12437.
30. Park CY, et al. (2009) STIM1 clusters and activates CRAC channels via direct binding of a cytosolic domain to Orai1. Cell 136(5):876-890.
31. Covington ED, Wu MM, Lewis RS (2010) Essential role for the CRAC activation domain in store-dependent oligomerization of STIM1. Mol Biol Cell 21(11):1897-1907.
32. Duman JG, Chen L, Palmer AE, Hille B (2006) Contributions of intracellular compartments to calcium dynamics: Implicating an acidic store. Traffic 7(7):859-872.
33. Docampo R, de Souza W, Miranda K, Rohloff P, Moreno SN (2005) Acidocalcisomes - Conserved from bacteria to man. Nat Rev Microbiol 3(3):251-261.
34. 2+) signaling: From phytoplankton to mammals. Cell Calcium 50(2):175-183.
35. 2+ homeostasis in human melanocytes. Pigment Cell Res 16(2):127-132.
36. Christensen KA, Myers JT, Swanson JA (2002) pH-dependent regulation of lysosomal calcium in macrophages. J Cell Sci 115(Pt 3):599-607.
37. Quesada I, Chin WC, Steed J, Campos-Bedolla P, Verdugo P (2001) Mouse mast cell secretory granules can function as intracellular ionic oscillators. Biophys J 80(5):2133-2139.
38. + from mast cell secretory granules: Implications for signal transduction. Biophys J 85(2):963-970.
39. 2+ release from bovine adrenal medullary secretory vesicles. J Biol Chem 265(23):13446-13448.
40. Yule DI, Ernst SA, Ohnishi H, Wojcikiewicz RJ (1997) Evidence that zymogen granules are not a physiologically relevant calcium pool. Defining the distribution of inositol 1,4,5-trisphosphate receptors in pancreatic acinar cells. J Biol Chem 272(14):9093-9098.
41. 2+ stores and associates with Orai1 upon depletion of the acidic stores in human platelets. J Biol Chem 286(14):12257-12270.
42. Lu X, Ellis-Davies GC, Levitan ES (2003) Calcium requirements for exocytosis do not delimit the releasable neuropeptide pool. Cell Calcium 33(4):267-271.
43. Feske S, et al. (2006) A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 441(7090):179-185.
44. Yang S, Zhang JJ, Huang XY (2009) Orai1 and STIM1 are critical for breast tumor cell migration and metastasis. Cancer Cell 15(2):124-134.
45. Zhang W, et al. (2011) Orai1-mediated I (CRAC) is essential for neointima formation after vascular injury. Circ Res 109(5):534-542.
46. Flourakis M, et al. (2010) Orai1 contributes to the establishment of an apoptosisresistant phenotype in prostate cancer cells. Cell Death Dis 1:e75.
47. 2 metabolism and KCNQ2/3 channel regulation studied with a voltage-sensitive phosphatase in living cells. J Gen Physiol 135(2):99-114.
48. Zhang B, Chenouard N, Olivo-Marin JC, Meas-Yedid V (2008) Statistical colocalization in biological imaging with false discovery control. Biomedical Imaging: From Nano to Macro (IEEE Conference Publications, Piscataway, NJ), pp 1327-1330.
49. Zhang Y, Chen L, Xu T (2010) Application of improved wavelet transform in biological particle detection. Prog Biochem Biophys 37(10):1144-1150.