Isoform- and species-specific control of inositol 1,4,5-trisphosphate (IP3) receptors by reactive oxygen species

Journal of Biological Chemistry

Volumn 289, Issue 12, 2014, Pages 8170-8181

  Bánsághi, Száva ^a   Golenár, Tünde ^a   Madesh, Muniswamy ^a   Csordás, György ^a   RamachandraRao, Satish ^a   Sharma, Kumar ^a   Yule, David I ^b   Joseph, Suresh K ^a   Hajnóczky, György ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; OXYGEN; RATS;

FREQUENCY-MODULATED OSCILLATION; MITOCHONDRIAL ENZYMES; MOLECULAR TARGETS; PERMEABILIZED CELLS; POTENTIAL TARGETS; REACTIVE OXYGEN SPECIES; SUPEROXIDE ANIONS; XANTHINE OXIDASE;

CALCIUM;

CALCIUM; IMMUNOGLOBULIN M; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; ISOPROTEIN; OXYGEN; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; XANTHINE; XANTHINE OXIDASE;

ANIMAL CELL; ARTICLE; CALCIUM MOBILIZATION; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL MEMBRANE PERMEABILITY; CHICKEN; COMPUTER MODEL; CONTROLLED STUDY; DOUBLE KNOCKOUT; ENDOPLASMIC RETICULUM; GENE INACTIVATION; HUMAN; HUMAN CELL; MITOCHONDRION; NONHUMAN; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTEIN METABOLISM; RAT; SENSITIZATION; TRIPLE KNOCKOUT;

CALCIUM SIGNALING; ENDOPLASMIC RETICULUM (ER); INOSITOL 1,4,5-TRISPHOSPHATE; IP3 RECEPTOR; MITOCHONDRIA; REACTIVE OXYGEN SPECIES (ROS);

AMINO ACID SEQUENCE; ANIMALS; CALCIUM SIGNALING; CELL LINE; CHICKENS; HUMANS; INOSITOL 1,4,5-TRISPHOSPHATE; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; PROTEIN ISOFORMS; RATS; REACTIVE OXYGEN SPECIES; SEQUENCE ALIGNMENT; SPECIES SPECIFICITY;

EID: 84897010947     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.504159     Document Type: Article

References (50)

1. Berridge, M. J. (2009) Inositol trisphosphate and calcium signalling mechanisms. Biochim. Biophys. Acta 1793, 933-940
2. Mikoshiba, K. (2007) IP3 receptor/Ca2+ channel: from discovery to new signaling concepts. J. Neurochem. 102, 1426-1446
3. Petersen, O. H., and Tepikin, A. V. (2008) Polarized calcium signaling in exocrine gland cells. Annu. Rev. Physiol. 70, 273-299 (Pubitemid 351738181)
4. Sanderson, M. J., Delmotte, P., Bai, Y., and Perez-Zogbhi, J. F. (2008) Regulation of airway smooth muscle cell contractility by Ca2+ signaling and sensitivity. Proc. Am. Thorac. Soc. 5, 23-31
5. Lewis, R. S. (2001) Calcium signaling mechanisms in T lymphocytes. Annu. Rev. Immunol. 19, 497-521
6. Malcuit, C., Kurokawa, M., and Fissore, R. A. (2006) Calcium oscillations and mammalian egg activation. J. Cell Physiol. 206, 565-573 (Pubitemid 43191029)
7. Szalai, G., Krishnamurthy, R., and Hajnóczky, G. (1999) Apoptosis driven by IP(3)-linked mitochondrial calcium signals. EMBO J. 18, 6349-6361 (Pubitemid 29533239)
8. Vanderheyden, V., Devogelaere, B., Missiaen, L., De Smedt, H., Bultynck, G., and Parys, J. B. (2009) Regulation of inositol 1,4,5-trisphosphate-induced Ca2+ release by reversible phosphorylation and dephosphorylation. Biochim. Biophys Acta 1793, 959-970
9. Betzenhauser, M. J., and Yule, D. I. (2010) Regulation of inositol 1,4,5-trisphosphate receptors by phosphorylation and adenine nucleotides. Curr. Top. Membr. 10.1016/S1063-5823(10)66012-7
10. Patterson, R. L., Boehning, D., and Snyder, S. H. (2004) Inositol 1,4,5-trisphosphate receptors as signal integrators. Ann. Rev. Biochem. 73, 437-465 (Pubitemid 39050376)
11. Joseph, S. K. (2010) Role of thiols in the structure and function of inositol trisphosphate receptors. Curr. Top. Membr. 66, 299-322
12. 2+ spikes in HeLa cells by sensitizing the inositol 1,4,5-trisphosphate receptor. J. Biol. Chem. 267, 25113-25119
13. 2+ flux through inositol 1,4,5-trisphosphate receptor type 1, but not type 3, via modulation of an isoform-specific Ca2+-dependent intramolecular interaction. Biochem. J. 381, 87-96
14. Khan, S. A., Rossi, A. M., Riley, A. M., Potter, B. V., and Taylor, C. W. (2013) Subtype-selective regulation of IP(3) receptors by thimerosal via cysteine residues within the IP(3)-binding core and suppressor domain. Biochem. J. 451, 177-184
15. Bird, G. S., Burgess, G. M., and Putney, J. W., Jr. (1993) Sulfhydryl reagents and cAMP-dependent kinase increase the sensitivity of the inositol 1,4,5-trisphosphate receptor in hepatocytes. J. Biol. Chem. 268, 17917-17923 (Pubitemid 23260306)
16. 2+ homeostasis in cultured aortic endothelial cells. Am. J. Physiol. Heart Circ. Physiol. 300, H493-H506
17. 2+ release via the IP3 receptor in cultured aortic endothelial cells. The J. Physiol. 590, 3431-3447
18. Joseph, S. K., Lin, C., Pierson, S., Thomas, A. P., and Maranto, A. R. (1995) Heteroligomers of type-I and type-III Inositol Trisphosphate receptors in WB rat liver epithelial cells. J. Biol. Chem. 270, 23310-23316
19. Wojcikiewicz, R. J., and He, Y. (1995) Type I, II and III Inositol 1,4,5-Trisphosphate receptor co-immunoprecipitation as evidence for the existence heterotetrameric receptor complexes. Biochem. Biophys. Res. Commun. 213, 334-341
20. Mendes, C. C., Gomes, D. A., Thompson, M., Souto, N. C., Goes, T. S., Goes, A. M., Rodrigues, M. A., Gomez, M. V., Nathanson, M. H., and Leite, M. F. (2005) The type III inositol 1,4,5-trisphosphate receptor preferentially transmits apoptotic Ca2+ signals into mitochondria. J. Biol. Chem. 280, 40892-40900 (Pubitemid 41780582)
21. Brown, G. C., and Borutaite, V. (2012) There is no evidence that mitochondria are the main source of reactive oxygen species in mammalian cells. Mitochondrion. 12, 1-4
22. Csordás, G., Thomas, A. P., and Hajnóczky, G. (1999) Quasi-synaptic calcium signal transmission between endoplasmic reticulum and mitochondria. EMBO J. 18, 96-108
23. Csordás, G., Renken, C., Várnai, P., Walter, L., Weaver, D., Buttle, K. F., Balla, T., Mannella, C. A., and Hajnóczky, G. (2006) Structural and functional features and significance of the physical linkage between ER and mitochondria. J. Cell Biol. 174, 915-921
24. Betzenhauser, M. J., Wagner, L. E., 2nd, Won, J. H., and Yule, D. I. (2008) Studying isoform-specific inositol 1,4,5-trisphosphate receptor function and regulation. Methods 46, 177-182
25. Leichert, L. I., and Jakob, U. (2004) Protein thiol modifications visualized in vivo. PLoS Biol. 2, e333
26. Csordás, G., and Hajnóczky, G. (2001) Sorting of calcium signals at the junctions of endoplasmic reticulum and mitochondria. Cell Calcium 29, 249-262
27. Pacher, P., Sharma, K., Csordás, G., Zhu, Y., and Hajnóczky, G. (2008) Uncoupling of ER-mitochondrial calcium communication by transforming growth factor-β. Am. J. Physiol. Renal Physiol. 295, F1303-1312
28. Akerboom, J., Carreras Calderón, N., Tian, L., Wabnig, S., Prigge, M., Tolö, J., Gordus, A., Orger, M. B., Severi, K. E., Macklin, J. J., Patel, R., Pulver, S. R., Wardill, T. J., Fischer, E., Schüler, C., Chen, T. W., Sarkisyan, K. S., Marvin, J. S., Bargmann, C. I., Kim, D. S., Kügler, S., Lagnado, L., Hegemann, P., Gottschalk, A., Schreiter, E. R., and Looger, L. L. (2013) Genetically encoded calcium indicators for multi-color neural activity imaging and combination with optogenetics. Front. Mol. Neurosci. 6, 2
29. Meyer, A. J., and Dick, T. P. (2010) Fluorescent protein-based redox probes. Antioxid. Redox Signal. 13, 621-650
30. Gutscher, M., Pauleau, A. L., Marty, L., Brach, T., Wabnitz, G. H., Samstag, Y., Meyer, A. J., and Dick, T. P. (2008) Real-time imaging of the intracellular glutathione redox potential. Nat. Methods 5, 553-559 (Pubitemid 351761764)
31. 2+ uniporter. Cell Metab. 17, 976-987
32. Madesh, M., and Hajnóczky, G. (2001) VDAC-dependent permeabilization of the outer mitochondrial membrane by superoxide induces rapid and massive cytochrome c release. J. Cell Biol. 155, 1003-1015 (Pubitemid 34286251)
33. Dooley, C. T., Dore, T. M., Hanson, G. T., Jackson, W. C., Remington, S. J., and Tsien, R. Y. (2004) Imaging dynamic redox changes in mammalian cells with green fluorescent protein indicators. J. Biol. Chem. 279, 22284-22293 (Pubitemid 38679425)
34. Hawkins, B. J., Madesh, M., Kirkpatrick, C. J., and Fisher, A. B. (2007) Superoxide flux in endothelial cells via the chloride channel-3 mediates intracellular signaling. Mol. Biol. Cell 18, 2002-2012 (Pubitemid 46911353)
35. Madesh, M., Hawkins, B. J., Milovanova, T., Bhanumathy, C. D., Joseph, S. K., Ramachandrarao, S. P., Sharma, K., Kurosaki, T., and Fisher, A. B. (2005) Selective role for superoxide in InsP3 receptor-mediated mitochondrial dysfunction and endothelial apoptosis. The J. Cell Biol. 170, 1079-1090 (Pubitemid 41362640)
36. Brookes, P. S., Yoon, Y., Robotham, J. L., Anders, M. W., and Sheu, S. S. (2004) Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am. J. Physiol. Cell Physiol. 287, C817-C833 (Pubitemid 39238305)
37. Higo, T., Hattori, M., Nakamura, T., Natsume, T., Michikawa, T., and Mikoshiba, K. (2005) Subtype-specific and ER lumenal environment-dependent regulation of inositol 1,4,5-trisphosphate receptor type 1 by ERp44. Cell 120, 85-98 (Pubitemid 40094605)
38. Enyedi, B., Várnai, P., and Geiszt, M. (2010) Redox state of the endoplasmic reticulum is controlled by Ero1L-α and intraluminal calcium. Antioxid. Redox Signal. 13, 721-729
39. Donoso, P., Sanchez, G., Bull, R., and Hidalgo, C. (2011) Modulation of cardiac ryanodine receptor activity by ROS and RNS. Front Biosci. 16, 553-567
40. 2+](i). J. Mol. Cell Cardiol. 58, 172-181
41. Voss, A. A., Lango, J., Ernst-Russell, M., Morin, D., and Pessah, I. N. (2004) Identification of hyperreactive cysteines within ryanodine receptor type 1 by mass spectrometry. J. Biol. Chem. 279, 34514-34520 (Pubitemid 39318079)
42. Aracena-Parks, P., Goonasekera, S. A., Gilman, C. P., Dirksen, R. T., Hidalgo, C., and Hamilton, S. L. (2006) Identification of cysteines involved in S-nitrosylation, S-glutathionylation, and oxidation to disulfides in ryanodine receptor type 1. J. Biol. Chem. 281, 40354-40368 (Pubitemid 46043301)
43. Petrotchenko, E. V., Yamaguchi, N., Pasek, D. A., Borchers, C. H., and Meissner, G. (2011) Mass spectrometric analysis and mutagenesis predict involvement of multiple cysteines in redox regulation of the skeletal muscle ryanodine receptor ion channel complex. Res. Rep. Biol 2011, 13-21
44. Sena, L. A., and Chandel, N. S. (2012) Physiological roles of mitochondrial reactive oxygen species. Mol. Cell 48, 158-167
45. Malhotra, J. D., and Kaufman, R. J. (2007) Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword? Antioxid. Redox Signal. 9, 2277-2293 (Pubitemid 350059010)
46. 2+ mobilisation in human platelets through sulphydryl oxidation dependent and independent mechanisms. Biochem. Pharmacol. 67, 491-502
47. Zheng, Y., and Shen, X. (2005) H2O2 directly activates inositol 1,4,5-trisphosphate receptors in endothelial cells. Redox Rep. 10, 29-36 (Pubitemid 41556828)
48. Thomas, A. P., Bird, G. S., Hajnóczky, G., Robb-Gaspers, L. D., and Putney, J. W., Jr. (1996) Spatial and temporal aspects of cellular calcium signaling. FASEB J. 10, 1505-1517 (Pubitemid 26384447)
49. Hajnóczky, G., and Thomas, A. P. (1997) Minimal requirements for calcium oscillations driven by the IP3 receptor. EMBO J. 16, 3533-3543 (Pubitemid 27250048)
50. Csordás, G., and Hajnóczky, G. (2009) SR/ER-mitochondrial local communication: calcium and ROS. Biochim. Biophys. Acta 1787, 1352-1362