Mitogenic signaling mediated by oxidants in Ras-transformed fibroblasts

Science

Volumn 275, Issue 5306, 1997, Pages 1649-1652

  Irani, Kaikobad ^a   Xia, Yong ^a   Zweier, Jay L ^a   Sollott, Steven J ^a   Der, Channing J ^b   Fearon, Eric R ^c   Sundaresan, Maitrayee ^d   Finkel, Toren ^d   Goldschmidt Clermont, Pascal J ^a,e  

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

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^d NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^e OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OXIDIZING AGENT;

ANIMAL CELL; ARTICLE; CANCER; CELL TRANSFORMATION; CHEMICAL CARCINOGENESIS; MITOGENESIS; MOUSE; NONHUMAN; ONCOGENE RAS; OXIDATIVE STRESS; PRIORITY JOURNAL;

3T3 CELLS; ACETYLCYSTEINE; ANIMALS; ANTIOXIDANTS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CELL CYCLE; CELL LINE, TRANSFORMED; CELL TRANSFORMATION, NEOPLASTIC; DNA; ELECTRON SPIN RESONANCE SPECTROSCOPY; GENES, RAS; GTP-BINDING PROTEINS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MICE; MITOGEN-ACTIVATED PROTEIN KINASES; OXIDATION-REDUCTION; PROTO-ONCOGENE PROTEINS P21(RAS); RAC GTP-BINDING PROTEINS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; SUPEROXIDES; TRANSFECTION;

ANIMALIA;

EID: 0030980641     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.275.5306.1649     Document Type: Article

References (53)

1. B. N. Ames, IARC Sci. Publ. 89, 407 (1988).
2. T. P. Szatrowski and C. F. Nathan, Cancer Res. 51, 794 (1991).
3. M. Sundaresan, Z.-X. Yu, V. J. Ferrans, K. Irani, T. Finkel, Science 270, 296 (1995); M. Ohba, M. Shibanuma, T. Kuroki, K. Nose, J. Cell Biol. 126, 1079 (1994); B. Meier et al., Biochem. J. 263, 539 (1989); Y. Y. C. Lo and T. F. Cruz, J. Biol. Chem. 270, 11727 (1995); A. Levine, R. Tenhaken, R. Dixon, C. Lamb, Cell 79, 583 (1994); G. B. Bulkley, Lancet 344, 934 (1994).
4. M. Sundaresan, Z.-X. Yu, V. J. Ferrans, K. Irani, T. Finkel, Science 270, 296 (1995); M. Ohba, M. Shibanuma, T. Kuroki, K. Nose, J. Cell Biol. 126, 1079 (1994); B. Meier et al., Biochem. J. 263, 539 (1989); Y. Y. C. Lo and T. F. Cruz, J. Biol. Chem. 270, 11727 (1995); A. Levine, R. Tenhaken, R. Dixon, C. Lamb, Cell 79, 583 (1994); G. B. Bulkley, Lancet 344, 934 (1994).
5. M. Sundaresan, Z.-X. Yu, V. J. Ferrans, K. Irani, T. Finkel, Science 270, 296 (1995); M. Ohba, M. Shibanuma, T. Kuroki, K. Nose, J. Cell Biol. 126, 1079 (1994); B. Meier et al., Biochem. J. 263, 539 (1989); Y. Y. C. Lo and T. F. Cruz, J. Biol. Chem. 270, 11727 (1995); A. Levine, R. Tenhaken, R. Dixon, C. Lamb, Cell 79, 583 (1994); G. B. Bulkley, Lancet 344, 934 (1994).
6. M. Sundaresan, Z.-X. Yu, V. J. Ferrans, K. Irani, T. Finkel, Science 270, 296 (1995); M. Ohba, M. Shibanuma, T. Kuroki, K. Nose, J. Cell Biol. 126, 1079 (1994); B. Meier et al., Biochem. J. 263, 539 (1989); Y. Y. C. Lo and T. F. Cruz, J. Biol. Chem. 270, 11727 (1995); A. Levine, R. Tenhaken, R. Dixon, C. Lamb, Cell 79, 583 (1994); G. B. Bulkley, Lancet 344, 934 (1994).
7. M. Sundaresan, Z.-X. Yu, V. J. Ferrans, K. Irani, T. Finkel, Science 270, 296 (1995); M. Ohba, M. Shibanuma, T. Kuroki, K. Nose, J. Cell Biol. 126, 1079 (1994); B. Meier et al., Biochem. J. 263, 539 (1989); Y. Y. C. Lo and T. F. Cruz, J. Biol. Chem. 270, 11727 (1995); A. Levine, R. Tenhaken, R. Dixon, C. Lamb, Cell 79, 583 (1994); G. B. Bulkley, Lancet 344, 934 (1994).
8. M. Sundaresan, Z.-X. Yu, V. J. Ferrans, K. Irani, T. Finkel, Science 270, 296 (1995); M. Ohba, M. Shibanuma, T. Kuroki, K. Nose, J. Cell Biol. 126, 1079 (1994); B. Meier et al., Biochem. J. 263, 539 (1989); Y. Y. C. Lo and T. F. Cruz, J. Biol. Chem. 270, 11727 (1995); A. Levine, R. Tenhaken, R. Dixon, C. Lamb, Cell 79, 583 (1994); G. B. Bulkley, Lancet 344, 934 (1994).
9. M. Rautalahti and J. Huttunen, Ann. Med. 25, 435 (1993); R. H. Burdon, V. Gill, D. Alliangana, Free Radical Res. Comm. 24, 81 (1996); R. H. Burdon and V. Gill, ibid. 19, 203 (1993); S. L. Church et al., Proc. Natl. Acad. Sci. U.S.A. 90, 3113 (1993).
10. M. Rautalahti and J. Huttunen, Ann. Med. 25, 435 (1993); R. H. Burdon, V. Gill, D. Alliangana, Free Radical Res. Comm. 24, 81 (1996); R. H. Burdon and V. Gill, ibid. 19, 203 (1993); S. L. Church et al., Proc. Natl. Acad. Sci. U.S.A. 90, 3113 (1993).
11. M. Rautalahti and J. Huttunen, Ann. Med. 25, 435 (1993); R. H. Burdon, V. Gill, D. Alliangana, Free Radical Res. Comm. 24, 81 (1996); R. H. Burdon and V. Gill, ibid. 19, 203 (1993); S. L. Church et al., Proc. Natl. Acad. Sci. U.S.A. 90, 3113 (1993).
12. M. Rautalahti and J. Huttunen, Ann. Med. 25, 435 (1993); R. H. Burdon, V. Gill, D. Alliangana, Free Radical Res. Comm. 24, 81 (1996); R. H. Burdon and V. Gill, ibid. 19, 203 (1993); S. L. Church et al., Proc. Natl. Acad. Sci. U.S.A. 90, 3113 (1993).
13. D. Diekmann, A. Abo, C. Johnston, A. W. Segal, A. Hall, Science 265, 531 (1994); G. M. Bokoch, Curr. Opin. Cell Biol. 6, 212 (1994); P. G. Heyworth et al., Mol. Biol. Cell 4, 1217 (1993); U. G. Knaus et al., J. Biol. Chem. 267, 23575 (1992); U. G. Knaus, P. G. Heyworth, T. Evans, J. T. Curnutte, G. M. Bokoch, Science 254, 1512 (1991); A. Abo et al., Nature 353, 668 (1991); T. Mizuno et al., J. Biol. Chem. 267, 10215 (1992).
14. D. Diekmann, A. Abo, C. Johnston, A. W. Segal, A. Hall, Science 265, 531 (1994); G. M. Bokoch, Curr. Opin. Cell Biol. 6, 212 (1994); P. G. Heyworth et al., Mol. Biol. Cell 4, 1217 (1993); U. G. Knaus et al., J. Biol. Chem. 267, 23575 (1992); U. G. Knaus, P. G. Heyworth, T. Evans, J. T. Curnutte, G. M. Bokoch, Science 254, 1512 (1991); A. Abo et al., Nature 353, 668 (1991); T. Mizuno et al., J. Biol. Chem. 267, 10215 (1992).
15. D. Diekmann, A. Abo, C. Johnston, A. W. Segal, A. Hall, Science 265, 531 (1994); G. M. Bokoch, Curr. Opin. Cell Biol. 6, 212 (1994); P. G. Heyworth et al., Mol. Biol. Cell 4, 1217 (1993); U. G. Knaus et al., J. Biol. Chem. 267, 23575 (1992); U. G. Knaus, P. G. Heyworth, T. Evans, J. T. Curnutte, G. M. Bokoch, Science 254, 1512 (1991); A. Abo et al., Nature 353, 668 (1991); T. Mizuno et al., J. Biol. Chem. 267, 10215 (1992).
16. D. Diekmann, A. Abo, C. Johnston, A. W. Segal, A. Hall, Science 265, 531 (1994); G. M. Bokoch, Curr. Opin. Cell Biol. 6, 212 (1994); P. G. Heyworth et al., Mol. Biol. Cell 4, 1217 (1993); U. G. Knaus et al., J. Biol. Chem. 267, 23575 (1992); U. G. Knaus, P. G. Heyworth, T. Evans, J. T. Curnutte, G. M. Bokoch, Science 254, 1512 (1991); A. Abo et al., Nature 353, 668 (1991); T. Mizuno et al., J. Biol. Chem. 267, 10215 (1992).
17. D. Diekmann, A. Abo, C. Johnston, A. W. Segal, A. Hall, Science 265, 531 (1994); G. M. Bokoch, Curr. Opin. Cell Biol. 6, 212 (1994); P. G. Heyworth et al., Mol. Biol. Cell 4, 1217 (1993); U. G. Knaus et al., J. Biol. Chem. 267, 23575 (1992); U. G. Knaus, P. G. Heyworth, T. Evans, J. T. Curnutte, G. M. Bokoch, Science 254, 1512 (1991); A. Abo et al., Nature 353, 668 (1991); T. Mizuno et al., J. Biol. Chem. 267, 10215 (1992).
18. D. Diekmann, A. Abo, C. Johnston, A. W. Segal, A. Hall, Science 265, 531 (1994); G. M. Bokoch, Curr. Opin. Cell Biol. 6, 212 (1994); P. G. Heyworth et al., Mol. Biol. Cell 4, 1217 (1993); U. G. Knaus et al., J. Biol. Chem. 267, 23575 (1992); U. G. Knaus, P. G. Heyworth, T. Evans, J. T. Curnutte, G. M. Bokoch, Science 254, 1512 (1991); A. Abo et al., Nature 353, 668 (1991); T. Mizuno et al., J. Biol. Chem. 267, 10215 (1992).
19. D. Diekmann, A. Abo, C. Johnston, A. W. Segal, A. Hall, Science 265, 531 (1994); G. M. Bokoch, Curr. Opin. Cell Biol. 6, 212 (1994); P. G. Heyworth et al., Mol. Biol. Cell 4, 1217 (1993); U. G. Knaus et al., J. Biol. Chem. 267, 23575 (1992); U. G. Knaus, P. G. Heyworth, T. Evans, J. T. Curnutte, G. M. Bokoch, Science 254, 1512 (1991); A. Abo et al., Nature 353, 668 (1991); T. Mizuno et al., J. Biol. Chem. 267, 10215 (1992).
20. B. Meier, A. R. Cross, J. T. Hancock, F. J. Kaup, O. T. G. Jones, Biochem. J. 275, 241 (1991); B. Meier, A. J. Jesaitis, A. Emmendorfer, J. Roesler, M. T. Quinn, ibid. 289, 481 (1993); H. I. Krieger-Brauer and H. Kather, ibid. 307, 549 (1995).
21. B. Meier, A. R. Cross, J. T. Hancock, F. J. Kaup, O. T. G. Jones, Biochem. J. 275, 241 (1991); B. Meier, A. J. Jesaitis, A. Emmendorfer, J. Roesler, M. T. Quinn, ibid. 289, 481 (1993); H. I. Krieger-Brauer and H. Kather, ibid. 307, 549 (1995).
22. B. Meier, A. R. Cross, J. T. Hancock, F. J. Kaup, O. T. G. Jones, Biochem. J. 275, 241 (1991); B. Meier, A. J. Jesaitis, A. Emmendorfer, J. Roesler, M. T. Quinn, ibid. 289, 481 (1993); H. I. Krieger-Brauer and H. Kather, ibid. 307, 549 (1995).
23. M. Barbacid, Annu. Rev. Biochem. 56, 779 (1987); J. L. Bos, Cancer Res. 49, 4682 (1989).
24. M. Barbacid, Annu. Rev. Biochem. 56, 779 (1987); J. L. Bos, Cancer Res. 49, 4682 (1989).
25. R. Qiu, J. Chen, D. Kim, F. McCormick, M. Symons, Nature 374, 457 (1995).
26. M. Sundaresan et al., Biochem. J. 318, 379 (1996).
27. A. W. Heldman et al., Circ. Res. 78, 312 (1996).
28. S. M. Oldham, G. J. Clark, L. M. Gangarosa, R. J. Coffey Jr., C. J. Der, Proc. Natl. Acad. Sci. U.S.A. 93, 6924 (1996).
29. J. L. Zweier et al., J. Biol. Chem. 269, 24156 (1994).
30. H. Gyllenhammar, J. Immunol. Methods 97, 209 (1987).
31. N. E. Kohl et al., Science 260, 1934 (1993); G. C. Pendergast et al., Mol. Cell. Biol. 14, 4193 (1994).
32. N. E. Kohl et al., Science 260, 1934 (1993); G. C. Pendergast et al., Mol. Cell. Biol. 14, 4193 (1994).
33. A. J. Ridley, H. F. Paterson, C. L. Johnston, D. Diekmann, A. Hall, Cell 70, 401 (1992); C. D. Nobes and A. Hall, ibid. 81, 53 (1995); A. J. Ridley and A. Hall, ibid. 70, 389 (1992).
34. A. J. Ridley, H. F. Paterson, C. L. Johnston, D. Diekmann, A. Hall, Cell 70, 401 (1992); C. D. Nobes and A. Hall, ibid. 81, 53 (1995); A. J. Ridley and A. Hall, ibid. 70, 389 (1992).
35. A. J. Ridley, H. F. Paterson, C. L. Johnston, D. Diekmann, A. Hall, Cell 70, 401 (1992); C. D. Nobes and A. Hall, ibid. 81, 53 (1995); A. J. Ridley and A. Hall, ibid. 70, 389 (1992).
36. L. S. Mulcahy, M. R. Smith, D. W. Stacey, Nature 313, 241 (1985); H. Cai, J. Szeberenyl, G. M. Cooper, Mol. Cell. Biol. 10, 5314 (1990).
37. L. S. Mulcahy, M. R. Smith, D. W. Stacey, Nature 313, 241 (1985); H. Cai, J. Szeberenyl, G. M. Cooper, Mol. Cell. Biol. 10, 5314 (1990).
38. K. Irani and P. J. Goldschmidt-Clermont, unpublished observations.
39. M. H. Cobb, T. G. Boulton, D. J. Robbins, Cell Regul. 2, 965 (1991); C. M. Crews and R. L. Erickson, Cell 74, 215 (1993).
40. M. H. Cobb, T. G. Boulton, D. J. Robbins, Cell Regul. 2, 965 (1991); C. M. Crews and R. L. Erickson, Cell 74, 215 (1993).
41. B. J. Pulverer et al., Nature 353, 670 (1991); H. Gille, A. D. Sharrocks, P. E. Shaw, ibid. 358, 414 (1992).
42. B. J. Pulverer et al., Nature 353, 670 (1991); H. Gille, A. D. Sharrocks, P. E. Shaw, ibid. 358, 414 (1992).
43. A. Minden et al., Cell 81, 1147 (1995); O. A. Coso et al., ibid., p. 1137; J. K, Westwick et al., Proc. Natl. Acad. Sci. U.S.A. 91, 6030 (1994); M. F. Olson, A. Ashworth, A. Hall, Science 269, 1270 (1995).
44. A. Minden et al., Cell 81, 1147 (1995); O. A. Coso et al., ibid., p. 1137; J. K, Westwick et al., Proc. Natl. Acad. Sci. U.S.A. 91, 6030 (1994); M. F. Olson, A. Ashworth, A. Hall, Science 269, 1270 (1995).
45. A. Minden et al., Cell 81, 1147 (1995); O. A. Coso et al., ibid., p. 1137; J. K, Westwick et al., Proc. Natl. Acad. Sci. U.S.A. 91, 6030 (1994); M. F. Olson, A. Ashworth, A. Hall, Science 269, 1270 (1995).
46. A. Minden et al., Cell 81, 1147 (1995); O. A. Coso et al., ibid., p. 1137; J. K, Westwick et al., Proc. Natl. Acad. Sci. U.S.A. 91, 6030 (1994); M. F. Olson, A. Ashworth, A. Hall, Science 269, 1270 (1995).
47. S. C. Erzurum, P. Lemarchand, M. A. Rosenfeld, J. Yoo, R. G. Crystal, Nucleic Acids Res. 21, 1607 (1993).
48. The spin trap DMPO (Aldrich, >97% pure) was used at 50 mM with the spectrometer set at a microwave frequency of 9.77 GHz with 20 mW of microwave power and a modulation amplitude of 0.5 G. Treatment with Cu-Zn SOD (Sigma), catalase (Sigma), DPI (Toronto Research), or N-acetyl-L-cysteine (Sigma) was for 20 min before recording of EPR spectra. Treatment with the FPTase inhibitor H-Ampamb-Phe-Met-OH (LC Laboratories) was for 48 hours before obtaining spectra. At this concentration and with this duration of treatment, no cellular toxicity was observed.
49. 5 cells. EPR spectra were obtained 48 hours after transfection. For the LUCL assay, 1 × 105 transfected cells were replated onto each tissue culture insert 24 hours after transfection and the assay was performed 24 hours later. Protein immunoblot analysis was done on cells 48 hours after transfection.
50. V12 in A6 cells was confirmed by protein immunoblotting with an antibody to H-Ras (Oncogene Science). Serum starvation was carried out in 0.1% serum for 48 hours.
51. 2, 15 mM Hepes, 10 mM EGTA (pH 7.0), 0.1% Triton X-100, 20 μg/ml each of chymostatin, pepstatin, antipain, and leupeptin, 1 mM 4-(2-aminoethyl)benzylsulfonyl fluoride, and 1 mM Na orthovanadate]. Immunoprecipitates or total cell lysates were subjected to SDS-polyacrylamide gel electrophoresis (PAGE) and transferred to nitrocellulose filters. Blots were then probed with the indicated antibody and developed by ECL (Amersham).
52. M. Hibi et al., Genes Dev. 7, 2135 (1993).
53. N17 cDNA, S. Erzurum for human catalase cDNA, and C. Lowenstein, C. Dang, and A. Hoang for helpful criticisms. Supported by NIH grant HL52315 (P.J.G.-C. and J.L.Z.), an Established Investigator Award, American Heart Association (P.J.G.-C.), and the Bernard Foundation.