Cytochrome c binds to inositol (1,4,5) trisphosphate receptors, amplifying calcium-dependent apoptosis

Nature Cell Biology

Volumn 5, Issue 12, 2003, Pages 1051-1061

  Boehning, Darren ^a   Patterson, Randen L ^a   Sedaghat, Leela ^a   Glebova, Natalia O ^a   Kurosaki, Tomohiro ^b   Snyder, Solomon H ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b KANSAI MEDICAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CYTOCHROME C; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR;

ANIMAL CELL; APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CALCIUM TRANSPORT; CONTROLLED STUDY; CYTOSOL; ENDOPLASMIC RETICULUM; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; SIGNAL TRANSDUCTION; STIMULUS RESPONSE;

ANIMALS; APOPTOSIS; BINDING SITES; BIOLOGICAL CLOCKS; CALCIUM; CALCIUM CHANNELS; CALCIUM SIGNALING; CYTOCHROMES C; CYTOSOL; ENDOPLASMIC RETICULUM; FEEDBACK, BIOCHEMICAL; HELA CELLS; HUMANS; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; MITOCHONDRIA; RATS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 0344825875     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/ncb1063     Document Type: Article

References (32)

1. Berridge, M. J., Lipp, P. & Bootman, M. D. The versatility and universality of calcium signalling. Nature Rev. Mol. Cell Biol. 1, 11-21 (2000).
2. Orrenius, S., Zhivotovsky, B. & Nicotera, P. Regulation of cell death: the calcium-apoptosis link. Nature Rev. Mol. Cell Biol. 4, 552-565 (2003).
3. Ferrari, D. et al. Endoplasmic reticulum, Bcl-2 and Ca(2+) handling in apoptosis. Cell Calcium 32, 413-420 (2002).
4. Hajnoczky, G., Csordas, G., Madesh, M. & Pacher, P. Control of apoptosis by IP(3) and ryanodine receptor driven calcium signals. Cell Calcium 28, 349-363 (2000).
5. Strasser, A., O'Connor, L. & Dixit, V. M. Apoptosis signaling. Annu. Rev. Biochem. 69, 217-245 (2000).
6. Goldstein, J. C., Waterhouse, N. J., Juin, P., Evan, G. I. & Green, D. R. The coordinate release of cytochrome c during apoptosis is rapid, complete and kinetically invariant. Nature Cell Biol. 2, 156-162 (2000).
7. Rizzuto, R. et al. Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses. Science 280, 1763-1766 (1998).
8. Csordas, G., Thomas, A. P. & Hajnoczky, G. Quasi-synaptic calcium signal transmission between endoplasmic reticulum and mitochondria. EMBO J. 18, 96-108 (1999).
9. Bezprozvanny, I., Watras, J. & Ehrlich, B. E. Bell-shaped calcium-response curves of Ins(1,4,5)P3- and calcium-gated channels from endoplasmic reticulum of cerebellum. Nature 351, 751-754 (1991).
10. Finch, E. A., Turner, T. J. & Goldin, S. M. Calcium as a coagonist of inositol 1,4,5-trisphosphate-induced calcium release. Science 252, 443-446 (1991).
11. Boehning, D. & Joseph, S. K. Functional properties of recombinant type I and type III inositol 1, 4,5-trisphosphate receptor isoforms expressed in COS-7 cells. J. Biol. Chem. 275, 21492-21499 (2000).
12. Tenhunen, R., Marver, H. S. & Schmid, R. The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc. Natl Acad. Sci. USA 61, 748-755 (1968).
13. Wojcikiewicz, R. J. Type I, II, and III inositol 1,4,5-trisphosphate receptors are unequally susceptible to down-regulation and are expressed in markedly different proportions in different cell types. J. Biol. Chem. 270, 11678-11683 (1995).
14. Diaz, F. & Bourguignon, L. Y. Selective down-regulation of IP(3)receptor subtypes by caspases and callpain during TNFα-induced apoptosis of human T-lymphoma cells. Cell Calcium 27, 315-328 (2000).
15. Hirota, J., Furuichi, T. & Mikoshiba, K. Inositol 1,4,5-trisphosphate receptor type 1 is a substrate for caspase-3 and is cleaved during apoptosis in a caspase-3-dependent manner. J. Biol. Chem. 274, 34433-34437 (1999).
16. Sugawara, H., Kurosaki, M., Takata, M. & Kurosaki, T. Genetic evidence for involvement of type 1, type 2 and type 3 inositol 1,4,5-trisphosphate receptors in signal transduction through the B-cell antigen receptor. EMBO J. 16, 3078-3088 (1997).
17. Ikonen, E., Fiedler, K., Parton, R. G. & Simons, K. Prohibitin, an antiproliferative protein, is localized to mitochondria. FEBS Lett. 358, 273-277 (1995).
18. Selvin, P. R., Fluorescence resonance energy transfer. Methods Enzymol. 246, 300-334 (1995).
19. Mochizuki, N. et al. Spatio-temporal images of growth-factor-induced activation of Ras and Rap1. Nature 411, 1065-1068 (2001).
20. Sorkin, A., McClure, M., Huang, F. & Carter, R. Interaction of EGF receptor and grb2 in living cells visualized by fluorescence resonance energy transfer (FRET) microscopy. Curr. Biol. 10, 1395-1398 (2000).
21. Hausmann, G. et al. Pro-apoptotic apoptosis protease-activating factor 1 (Apaf-1) has a cytoplasmic localization distinct from Bcl-2 or Bcl-x(L). J. Cell Biol. 149, 623-634 (2000).
22. Okazaki, M., Ishibashi, Y., Asoh, S. & Ohta, S. Overexpressed mitochondrial hinge protein, a cytochrome c-binding protein, accelerates apoptosis by enhancing the release of cytochrome c from mitochondria. Biochem. Biophys. Res. Commun. 243, 131-136 (1998).
23. Jayaraman, T. & Marks,A. R. T cells deficient in inositol 1,4,5-trisphosphate receptor are resistant to apoptosis. Mol. Cell Biol. 17, 3005-3012 (1997).
24. Blackshaw, S. et al. Type 3 inositol 1,4,5-trisphosphate receptor modulates cell death. FASEB J. 14, 1375-1379 (2000).
25. Khan, A. A. et al. Lymphocyte apoptosis: mediation by increased type 3 inositol 1,4,5-trisphosphate receptor, Science 273, 503-507 (1996).
26. Marsden, V. S. et al. Apoptosis initiated by Bcl-2-regulated caspase activation independently of the cytochrome c/Apaf-1/caspase-9 apoptosome. Nature 419, 634-637 (2002).
27. Lassus, P., Opitz-Araya, X. & Lazebnik, Y. Requirement for caspase-2 in stress-induced apoptosis before mitochondrial permeabilization. Science 297, 1352-1354 (2002).
28. Boehning, D. & Joseph, S. K. Direct association of ligand-binding and pore domains in homo- and heterotetrameric inositol 1,4,5-trisphosphate receptors. EMBO J. 19, 5450-5459 (2000).
29. Joseph, S. K. & Samanta, S. Detergent solubility of the inostol trisphosphate receptor in rat brain membranes. Evidence for association of the receptor with ankyrin.PG. J. Biol. Chem. 268, 6477-6486 (1993).
30. Dore, S. et al. Bilirubin, formed by activation of heme oxygenase-2, protects neurons against oxidative stress injury. Proc. Natl Acad. Sci. USA 96, 2445-2450 (1999).
31. Ferris, C. D., Cameron, A. M., Huganir, R. L. & Snyder, S. H. Quantal calcium release by purified reconstituted inositol 1,4,5- trisphosphate receptors. Nature 356, 350-352 (1992).
32. 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).