Requirement of JNK for stress-induced activation of the cytochrome c- mediated death pathway

Science

Volumn 288, Issue 5467, 2000, Pages 870-874

  Tournier, Cathy ^a   Hess, Patricia ^a   Yang, Derek D ^b,d   Xu, Jie ^b   Turner, Tod K ^a   Nimnual, Anjaruwee ^c   Bar Sagi, Dafna ^c   Jones, Stephen N ^a   Flavell, Richard A ^b   Davis, Roger J ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c STONY BROOK UNIVERSITY   (United States)

^d ELI LILLY AND COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL CELL; APOPTOSIS; ARTICLE; ENZYME ACTIVATION; FIBROBLAST; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ULTRAVIOLET RADIATION;

ANIMALS; APOPTOSIS; APOPTOTIC PROTEASE-ACTIVATING FACTOR 1; CASPASE 3; CASPASE 9; CASPASES; CELL COUNT; CELL DIVISION; CELLS, CULTURED; CYTOCHROME C GROUP; DNA FRAGMENTATION; ENZYME ACTIVATION; FIBROBLASTS; GENE TARGETING; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE SIGNALING SYSTEM; METHYL METHANESULFONATE; MICE; MITOCHONDRIA; MITOGEN-ACTIVATED PROTEIN KINASES; NF-KAPPA B; PROTEIN-SERINE-THREONINE KINASES; PROTEINS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-BCL-2; TUMOR SUPPRESSOR PROTEIN P53; ULTRAVIOLET RAYS;

ANIMALIA; MURINAE;

EID: 0034607702     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.288.5467.870     Document Type: Article

References (51)

1. D. L. Vaux and S. J. Korsmeyer, Cell 96, 245 (1999).
2. G. Evan and T. Littlewood, Science 281, 1317 (1998); J. Yuan and B. A. Yankner, Nature Cell Biol. 1, E44 (1999).
3. G. Evan and T. Littlewood, Science 281, 1317 (1998); J. Yuan and B. A. Yankner, Nature Cell Biol. 1, E44 (1999).
4. D. D. Yang et al., Nature 389, 865 (1997).
5. D. D. Yang et al., Immunity 9, 575 (1998); C. Dong et al., Science 282, 2092 (1998); C. Y. Kuan et al., Neuron 22, 667 (1999).
6. D. D. Yang et al., Immunity 9, 575 (1998); C. Dong et al., Science 282, 2092 (1998); C. Y. Kuan et al., Neuron 22, 667 (1999).
7. D. D. Yang et al., Immunity 9, 575 (1998); C. Dong et al., Science 282, 2092 (1998); C. Y. Kuan et al., Neuron 22, 667 (1999).
8. C. Tournier, unpublished observation.
9. R. S. Johnson et al., Genes Dev. 7, 1309 (1993); M. Schreiber et al., Genes Dev. 13, 607 (1999).
10. R. S. Johnson et al., Genes Dev. 7, 1309 (1993); M. Schreiber et al., Genes Dev. 13, 607 (1999).
11. A. Behrens, M. Sibilia, E. F. Wagner, Nature Genet. 21, 325 (1999).
12. Y. T. Ip and R. J. Davis, Curr. Opin. Cell Biol. 10, 205 (1998).
13. M. Dickens et al., Science 277, 693 (1997); Z. Xia et al., Science 270, 1326 (1995).
14. M. Dickens et al., Science 277, 693 (1997); Z. Xia et al., Science 270, 1326 (1995).
15. G. Natoli et al., Science 275, 200 (1997); Z. G. Liu et al., Cell 87, 565 (1996); A. Roulston et al., J. Biol. Chem. 273, 10232 (1998).
16. G. Natoli et al., Science 275, 200 (1997); Z. G. Liu et al., Cell 87, 565 (1996); A. Roulston et al., J. Biol. Chem. 273, 10232 (1998).
17. G. Natoli et al., Science 275, 200 (1997); Z. G. Liu et al., Cell 87, 565 (1996); A. Roulston et al., J. Biol. Chem. 273, 10232 (1998).
18. A. Khwaja, Nature 401, 33 (1999).
19. J. Downward, Curr. Opin. Cell Biol. 10, 262 (1998).
20. S. Y. Fuchs et al., Genes Dev. 12, 2658 (1998).
21. A. J. Giaccia and M. B. Kastan, Genes Dev. 12, 2973 (1998).
22. J. D. Weber et al., Nature Cell Biol. 1, 20 (1999).
23. B. B. Wolf and D. R. Green, J. Biol. Chem. 274, 20049 (1999).
24. P. Juo et al., Curr. Biol. 8, 1001 (1998); E. E. Varfolomeev et al., Immunity 9, 267 (1998).
25. P. Juo et al., Curr. Biol. 8, 1001 (1998); E. E. Varfolomeev et al., Immunity 9, 267 (1998).
26. M. Woo et al., Genes Dev. 12, 806 (1998); K. Kuida et al., Nature 384, 358 (1996).
27. M. Woo et al., Genes Dev. 12, 806 (1998); K. Kuida et al., Nature 384, 358 (1996).
28. R. Hakem et al., Cell 94, 339 (1998); K. Kuida et al., Cell 94, 325 (1998).
29. R. Hakem et al., Cell 94, 339 (1998); K. Kuida et al., Cell 94, 325 (1998).
30. F. Cecconi et al., Cell 94, 727 (1998); H. Yoshida et al., Cell 94, 739 (1998).
31. F. Cecconi et al., Cell 94, 727 (1998); H. Yoshida et al., Cell 94, 739 (1998).
32. H. Zou et al., Cell 90, 405 (1997); P. Li et al., Cell 91, 479 (1997).
33. H. Zou et al., Cell 90, 405 (1997); P. Li et al., Cell 91, 479 (1997).
34. A. Gross, J. M. McDonnell, S. J. Korsmeyer, Genes Dev. 13, 1899 (1999).
35. K. Yamamoto, H. Ichijo, S. J. Korsmeyer, Mol. Cell. Biol. 19, 8469 (1999); R. K. Srivastava et al., Proc. Natl. Acad. Sci. U.S.A. 96, 3775 (1999); K. Maundrell et al., J. Biol. Chem. 272, 25238 (1997); S. Haldar, N. Jena, C. M. Croce, Proc. Natl. Acad. Sci. U.S.A. 92, 4507 (1995).
36. K. Yamamoto, H. Ichijo, S. J. Korsmeyer, Mol. Cell. Biol. 19, 8469 (1999); R. K. Srivastava et al., Proc. Natl. Acad. Sci. U.S.A. 96, 3775 (1999); K. Maundrell et al., J. Biol. Chem. 272, 25238 (1997); S. Haldar, N. Jena, C. M. Croce, Proc. Natl. Acad. Sci. U.S.A. 92, 4507 (1995).
37. K. Yamamoto, H. Ichijo, S. J. Korsmeyer, Mol. Cell. Biol. 19, 8469 (1999); R. K. Srivastava et al., Proc. Natl. Acad. Sci. U.S.A. 96, 3775 (1999); K. Maundrell et al., J. Biol. Chem. 272, 25238 (1997); S. Haldar, N. Jena, C. M. Croce, Proc. Natl. Acad. Sci. U.S.A. 92, 4507 (1995).
38. K. Yamamoto, H. Ichijo, S. J. Korsmeyer, Mol. Cell. Biol. 19, 8469 (1999); R. K. Srivastava et al., Proc. Natl. Acad. Sci. U.S.A. 96, 3775 (1999); K. Maundrell et al., J. Biol. Chem. 272, 25238 (1997); S. Haldar, N. Jena, C. M. Croce, Proc. Natl. Acad. Sci. U.S.A. 92, 4507 (1995).
39. X. M. Yin et al., Nature 400, 886 (1999); H. Li, H. Zhu, C. J. Xu, J. Yuan, Cell 94, 491 (1998); X. Luo et al., Cell 94, 481 (1998).
40. X. M. Yin et al., Nature 400, 886 (1999); H. Li, H. Zhu, C. J. Xu, J. Yuan, Cell 94, 491 (1998); X. Luo et al., Cell 94, 481 (1998).
41. X. M. Yin et al., Nature 400, 886 (1999); H. Li, H. Zhu, C. J. Xu, J. Yuan, Cell 94, 491 (1998); X. Luo et al., Cell 94, 481 (1998).
42. E. Bossy-Wetzel, D. D. Newmeyer, D. R. Green, EMBO J. 17, 37 (1998).
43. MEF were prepared from day 13.5 embryos and cultured in Dulbecco's modified Eagle's medium supplemented with 10% fetal bovine serum (Life Technologies). All experiments were done with cells between passage 2 and passage 5. Similar data were obtained in experiments with independently isolated MEF.
44. Frozen cell pellets were lysed on ice (30 min) in RIPA buffer [50 mM tris-HCl (pH 7.5), 10 mM β-glycerophosphate, 5 mM EDTA, 150 mM NaCl, 1% Nonidet P-40, 1 mM phenylmethylsulfonyl fluoride, 1 mM sodium orthovanadate, aprotinin at 0.4 unit/ml, and leupeptin at 0.4 unit/ml]. Extracts (100 μg of protein) were examined by protein immunoblot analysis by probing with antibodies to PKB/AKT (New England Biolabs), p38 MAPK (Santa Cruz), ERK (Santa Cruz), JNK (Pharmingen), MKK4 (Santa Cruz), MKK7 (Zymed), p53 (Calbiochem), p73 (provided by W. G. Kaelin Jr.), ARF (Novus Biologicals), caspase 3 (Santa Cruz), active caspase 3 [A. Srinivasan et al., Cell Death Differ. 5, 1004 (1998)], p21 (Santa Cruz), Bd2 (Pharmingen), Bax (Pharmingen), and actin (Calbiochem). S100 fractions were prepared [J. Yang et al., Science 275, 1129 (1997)] and examined by immunoblot analysis by probing with antibodies to cytochrome c (Pharmingen) and Bid (provided by X. Wang). Immune complexes were detected by enhanced chemiluminescence (Kirkegaard & Perry).
45. Frozen cell pellets were lysed on ice (30 min) in RIPA buffer [50 mM tris-HCl (pH 7.5), 10 mM β-glycerophosphate, 5 mM EDTA, 150 mM NaCl, 1% Nonidet P-40, 1 mM phenylmethylsulfonyl fluoride, 1 mM sodium orthovanadate, aprotinin at 0.4 unit/ml, and leupeptin at 0.4 unit/ml]. Extracts (100 μg of protein) were examined by protein immunoblot analysis by probing with antibodies to PKB/AKT (New England Biolabs), p38 MAPK (Santa Cruz), ERK (Santa Cruz), JNK (Pharmingen), MKK4 (Santa Cruz), MKK7 (Zymed), p53 (Calbiochem), p73 (provided by W. G. Kaelin Jr.), ARF (Novus Biologicals), caspase 3 (Santa Cruz), active caspase 3 [A. Srinivasan et al., Cell Death Differ. 5, 1004 (1998)], (Santa Cruz), Bd2 (Pharmingen), Bax (Pharmingen), and actin (Calbiochem). S100 fractions were prepared [J. Yang et al., Science 275, 1129 (1997)] and examined by immunoblot analysis by probing with antibodies to cytochrome c (Pharmingen) and Bid (provided by X. Wang). Immune complexes were detected by enhanced chemiluminescence (Kirkegaard & Perry).
46. 2 (Alexis Biochemicals) and analyzing by flow cytometry [D. M. Finucane et al., J. Biol. Chem. 274, 2225 (1999)].
47. 2 (Alexis Biochemicals) and analyzing by flow cytometry [D. M. Finucane et al., J. Biol. Chem. 274, 2225 (1999)].
48. 2 (Alexis Biochemicals) and analyzing by flow cytometry [D. M. Finucane et al., J. Biol. Chem. 274, 2225 (1999)].
49. 2 (Alexis Biochemicals) and analyzing by flow cytometry [D. M. Finucane et al., J. Biol. Chem. 274, 2225 (1999)].
50. Cells were plated onto gridded cover slips and maintained in Dulbecco's modified Eagle's medium containing 10% fetal calf serum for 2 days before injection. Fluorescein-conjugated dextran and cytochrome c (Sigma) were dissolved in phosphate-buffered saline and microinjected into the cytoplasm. Injected cells were identified by fluorescence microscopy and apoptosis was quantified by counting the number of injected cells immediately after injection and again 2 hours after injection. Apoptotic MEF aggregate and rapidly detach from the cover slip, which makes it impossible to score for individual apoptotic cells.
51. Supported in part by a grant from the National Cancer Institute. We thank our colleagues for providing reagents essential for this study, M. Woda for assistance with fluorescence-activated cell sorter analysis, and Kathy Gemme for expert administrative assistance. R.A.F. and R.J.D. are investigators of the Howard Hughes Medical Institute.