Selective localization of Bcl-2 to the inner mitochondrial and smooth endoplasmic reticulum membranes in mammalian cells

Cell Death and Differentiation

Volumn 7, Issue 7, 2000, Pages 666-674

  Gotow, T ^a   Shibata, M ^b   Kanamori, S ^b   Tokuno, O ^b   Ohsawa, Y ^b   Sato, N ^b   Isahara, K ^b   Yayoi, Y ^b   Watanabe, T ^b   Leterrier, J F ^c   Linden, M ^c   Kominami, E ^d   Uchiyama, Yasuo ^b  

^a KOSHIEN UNIVERSITY   (Japan)

^b OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c CNRS   (France)

^d JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Apoptosis; Bcl 2; Mitochondria; PC12 cells; Rat brains; Smooth endoplasmic reticulum

Indexed keywords

MEMBRANE PROTEIN; PROTEIN BCL 2; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

ANIMAL CELL; ARTICLE; BRAIN; CELL CULTURE; CONTROLLED STUDY; DNA TRANSFECTION; ENDOPLASMIC RETICULUM; ENZYME SUBUNIT; IMMUNOHISTOCHEMISTRY; MAMMAL CELL; MITOCHONDRIAL MEMBRANE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT;

ANIMALIA; MAMMALIA;

EID: 0033939697     PISSN: 13509047     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.cdd.4400694     Document Type: Article

References (45)

1. Tsujimoto Y, Gorham J, Cossman J, Jaffe E and Croce CM (1985) The t(14;18) chromosome translocations involved in B-cell neoplasms result from mistakes in VDJ joining. Science 229: 1390-1393
2. H on chromosome 14 and near a transcriptional unit on 18. Cell 41: 899-906
3. Cleary ML and Sklar J (1985) Nucleotide sequence of a t(14;18) chromosomal breakpoint in follicular lymphoma and demonstration of a breakpoint in follicular lymphoma and demonstration of a breakpoint-cluster region near a transcriptionally active locus on chromosome 18. Proc. Natl. Acad. Sci. USA 82: 7439-7443
4. Gross A, McDonnell JM and Korsmeyer SJ (1999) BCL-2 family members and the mitochondria in apoptosis. Genes Dev. 13: 1899-1911
5. Scaffidi C, Fulda S, Srinivasan A, Friesen C, Li F, Tomaselli KJ, Debatin KM, Krammer PH and Peter ME (1998) Two CD95 (APO-1/Fas) signaling pathways. EMBO J. 17: 1675-1687
6. Chen-Levy Z, Nourse J and Cleary ML (1989) The bcl-2 candidate protooncogene product is a 24-kilodalton integral-membrane protein highly expressed in lymphoid cell lines and lymphomas carrying the t(14;18) translocation. Mol. Cell Biol. 9: 701-710
7. Chen-Levy Z and Cleary ML (1990) Membrane topology of the Bcl-2 protooncogenic protein demonstrated in vitro. J. Biol. Chem. 265: 4929-4933
8. Nguyen M, Millar DG, Yong VW, Korsmeyer SJ and Shore GC (1993) Targeting of Bcl-2 to the mitochondrial outer membrane by a COOH-term nal signal anchor sequence. J. Biol. Chem. 268: 25265-25268
9. Baffy G, Miyashita T, Williamson JR and Reed JC (1993) Apoptotis induced by withdrawal of interleukin-3 (IL-3) from an IL-3-dependent hematopoietic cell line is associated with repartitioning of intracellular calcium and is blocked by enforced Bcl-2 oncoprotein production. J. Biol. Chem. 268: 6511-6519
10. 2+ fluxes. Proc. Natl. Acad. Sci. USA 91: 6569-6573
11. Ryan JJ, Prochownik E, Gottlieb CA, Apel IJ, Merino R, Nunez G and Clarke MF (1994) c-myc and bcl-2 modulate p53 function by altering p53 subcellular trafficking during the cell cycle. Proc. Natl. Acad. Sci. USA 91: 5878-5882
12. Krajewski S, Tanaka S, Takayama S, Schibler MJ, Fenton Wand Reed JC (1993) Investigation of the subcellular distribution of the bcl-2 oncoprotein: residence in the nuclear envelope, endoplasmic reticulum, and outer mitochondrial membranes. Cancer Res. 53: 4701-4714
13. Akao Y, Otuski Y, Kataoka S, Ito Y and Tsujimoto Y (1994) Multiple subcellular localization of bcl-2: detection in nuclear outer membrane, endoplasmic reticulum membrane, and mitochondrial membranes. Cancer Res. 54: 2468-2471
14. Shimizu S, Narita M and Tsujimoto Y (1999) Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature 399: 483-487
15. Häcker G and Vaux DL (1995) Apoptosis. A sticky business. Curr. Biol. 5: 622-624
16. Yang E, Zha J, Jockel J, Boise LH, Thompson CB and Korsmeyer SL (1995) Bad, a heterodimeric partner for Bcl-xL and Bcl-2, displaces Bax and promotes cell death. Cell 80: 285-291
17. Wang HG, Rapp UR and Reed JC (1996) Bcl-2 targets the protein kinase Raf-1 to mitochondria. Cell 87: 629-638
18. Wang HG, Takayam S, Rapp UR and Reed JC (1996) Bcl-2 interacting protein, BAG-1, binds to and activates the kinase Raf-1. Proc. Natl. Acad. Sci. USA 93: 7063-7068
19. 2+)-activated cell death in mammalian cells. J. Cell Biol. 131: 735-743
20. Reed JC (1997) Double identity for proteins of the Bcl-2 family. Nature 387: 773-776
21. Kluck RM, Bossy-Wetzel E, Green DR and Evan GI (1997) The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275: 1132-1136
22. Yang J, Liu X , Bhalla K, Kim CN, Ibrado AM, Cai J, Peng TI, Jones DP and Wang X (1997) Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275: 1129-1132
23. Motoyama S, Kitamura M, Saito S, Minamiya Y, Suzuki H, Saito R, Terada K, Ogawa J and Inaba H (1998) Bcl-2 is located predominantly in the inner membrane and crista of mitochondria in rat liver. Biochem. Biophys. Res. Commun. 249: 628-636
24. Kharbanda S, Pandey P, Schofield L, Israels S, Roncinske R, Yoshida, Bharti A, Yuan ZM, Saxena S, Weichselbaum R, Nalin C and Kufe D (1997) Role for Bcl-xL, as an inhibitor of cytosolic cytochrome c accumulation in DNA damage-induced apoptosis. Proc. Natl. Acad. Sci. USA 94: 6939-6942
25. Hockenbery DM, Nuñez G, Milliman C, Schreiber RD and Korsmeyer SJ (1990) Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature 348: 334-336
26. Shimizu S, Eguchi Y, Kamiike W, Waguri S, Uchiyama Y, Matsuda H and Tsujimoto Y (1996) Bcl-2 blocks loss of mitochondrial membrane potential while ICE inhibitors act at a different step during inhibition of death induced by respiratory chain inhibitors. Oncogene 13: 21-29
27. Zamzami N, Susin SA, Marchetti P, Hirsch T, Gómez-Monterrey I, Castedo M and Kroemer G (1996) Mitochondrial control of nuclear apoptosis. J. Exp. Med. 183: 1533-1544
28. Iwahashi J, Yamazaki S, Komiya T, Nomura N, Nishikawa S, Endo T and Mihara K (1997) Analysis of the functional domain of the rat liver mitochondrial import receptor Tom20. J. Biol. Chem. 272: 18467-18472
29. Monaghan P, Robertso D, Amos TAS, Dyer MJS, Mason DY and Greaves MF (1992) Ultrastructural localization of Bcl-2 protein. J. Histochem. Cytochem. 40: 1819-1825
30. Nakai M, Takeda A, Cleary ML and Endo T (1993) The Bcl-2 protein is inserted into the outer membrane but not into the inner membrane of rat liver mitochondria in vitro. Biochem. Biophys. Res. Commun. 196: 233-239
31. Jong de D, Prins FA, Mason DY, Reed JC, Ommen van GB and Kluin PM (1994) Subcellular localization of the bcl-2 protein in malignant and normal lymphoid cells. Cancer Res. 54: 256-260
32. Jacobson MD, Burne JF, King MP, Miyashita T, Reed JC and Raff MC (1993) Bcl-2 blocks apoptosis in cells lacking mitochondrial DNA. Nature 361: 365-369
33. Alnemri ES, Robertson NM, Fernandes TR, Croce CM and Litwack G (1992) Overexpressed full-length human BCL2 extends the survival of baculovirus-infected Sf9 insect cells. Proc. Natl. Acad. Sci. USA 89: 7295-7299
34. Dorbani L, Jancsik V, Linden M, Leterrier JF, Nelson BD and Rendon A (1987) Subfractionation of the outer membrane of rat brain mitochondria: Evidence for the existence of a domain containing the porin-hexokinase complex. Arch. Biochem. Biophys. 252: 188-196
35. Jancsik V, Lindén M, Dorbani L, Rendon A and Nelson BD (1988) Studies of the relationship between the inner and the outer membrane from rat liver mitochondria as determined by subfractionation with digitonin. Arch. Biochem. Biophys. 264: 295-301
36. Liu X, Kim CN, Yang J, Jemmerson R and Wang X (1996) Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86: 147-157
37. Green DR and Reed JC (1998) Mitochondria and apoptosis. Science 281: 1309-1312
38. Sato N, Hotta K, Waguri S, Nitatori T, Tohyama K, Tsujimoto Y and Uchiyama Y (1994) Neuronal differentiation of PC 12 cells as a result of prevention of cell death by bcl-2. J. Neurobiol. 25: 1227-1234
39. Pezzella F, Tse AG, Cordell JL, Pulford KA, Gatter KC and Mason DY (1990) Expression of the bcl-2 oncogene protein is not specific for the 14;18 chromosomal translocation. Am. J. Pathol. 137: 225-232
40. Esaki J, Wilfe LS and Kominami E (1996) Specific delay in the degradation of mitochondrial ATP synthase subunit c in late infantile neuronal ceroid lipofuscinosis is derived from cellular proteolytic dysfunction rather than structural alteration of subunit c. J. Neurochem. 67: 1677-1687
41. Lindén M, Andersson G, Gellerfors P and Nelson BD (1984) Subcellular distribution of rat liver porin. Biochem. Biophys. Acta 770: 93-96
42. Ohsawa Y, Isahara K, Kanamori S, Shibata M, Kametaka S, Gotow T, Watanabe T, Kominami E and Uchiyama Y (1988) Ultrastructural and immunohistochemical study of PC12 cells during apoptosis induced by serum deprivation with special reference to autophagy and lysosomal cathepsins. Arch. Histol. Cytol. 61: 395-403
43. Gotow T, Sakata M, Funakoshi T and Uchiyama Y (1996) Preferential localization of annexin V to the axon terminal. Neuroscience 75: 507-521
44. Tokuyasu KT (1980) Immunocytochemistry on ultrathin frozen section. Histochem. J. 12: 381-403
45. Storrie B and Madden EA (1990) Isolation of subcellular organelles. Method Enzymol. 182: 203-225