PKC regulates a farnesyl-electrostatic switch on K-Ras that promotes its association with Bcl-XL on mitochondria and induces apoptosis

Molecular Cell

Volumn 21, Issue 4, 2006, Pages 481-493

  Bivona, Trever G ^a   Quatela, Steven E ^a   Bodemann, Brian O ^b   Ahearn, Ian M ^a   Soskis, Michael J ^a   Mor, Adam ^a   Miura, John ^a   Wiener, Heidi H ^a   Wright, Latasha ^a   Saba, Shahryar G ^a   Yim, Duke ^a   Fein, Adam ^a   Pérez De Castro, Ignacio ^a,d   Li, Chi ^c   Thompson, Craig B ^c   Cox, Adrienne D ^b   Philips, Mark R ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

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

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d Structural Biology and Biocomputing Programme   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BRYOSTATIN 1; PROTEIN BCL XL; PROTEIN KINASE C;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL MEMBRANE; CELL TRANSFORMATION; CONTROLLED STUDY; ELECTRICITY; GENE CONTROL; GENE FUNCTION; GENE LOCATION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; ONCOGENE K RAS; PROMOTER REGION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; WILD TYPE;

AMINO ACID SEQUENCE; ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BCL-X PROTEIN; CELL LINE; CELL MEMBRANE; ELECTROSTATICS; GENES, RAS; HUMANS; INTRACELLULAR MEMBRANES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MACROLIDES; MEMBRANE PROTEINS; MICE; MICE, NUDE; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; NEOPLASMS; PROTEIN ISOFORMS; PROTEIN KINASE C; RECOMBINANT FUSION PROTEINS; SERINE; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

ANIMALIA;

EID: 32444441115     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2006.01.012     Document Type: Article

References (45)

1. R. Ballester, M.E. Furth, and O.M. Rosen Phorbol ester- and protein kinase C-mediated phosphorylation of the cellular Kirsten ras gene product J. Biol. Chem. 262 1987 2688 2695
2. T.G. Bivona, I. Perez De Castro, I.M. Ahearn, T.M. Grana, V.K. Chiu, P.J. Lockyer, P.J. Cullen, A. Pellicer, A.D. Cox, and M.R. Philips Phospholipase Cγ activates Ras on the Golgi apparatus by means of RasGRP1 Nature 424 2003 694 698
3. J.L. Bos ras oncogenes in human cancer: a review Cancer Res. 49 1989 4682 4689
4. D.G. Breckenridge, M. Germain, J.P. Mathai, M. Nguyen, and G.C. Shore Regulation of apoptosis by endoplasmic reticulum pathways Oncogene 22 2003 8608 8618
5. V.K. Chiu, T. Bivona, A. Hach, J.B. Sajous, J. Silletti, H. Wiener, R.L. Johnson, A.D. Cox, and M.R. Philips Ras signalling on the endoplasmic reticulum and the Golgi Nat. Cell Biol. 4 2002 343 350
6. J.A. Choi, M.T. Park, C.M. Kang, H.D. Um, S. Bae, K.H. Lee, T.H. Kim, J.H. Kim, C.K. Cho, and Y.S. Lee Opposite effects of Ha-Ras and Ki-Ras on radiation-induced apoptosis via differential activation of PI3K/Akt and Rac/p38 mitogen-activated protein kinase signaling pathways Oncogene 23 2004 9 20
7. E. Choy, V.K. Chiu, J. Silletti, M. Feoktistov, T. Morimoto, D. Michaelson, I.E. Ivanov, and M.R. Philips Endomembrane trafficking of ras: the CAAX motif targets proteins to the ER and Golgi Cell 98 1999 69 80
8. A.D. Cox, and C.J. Der The dark side of Ras: regulation of apoptosis Oncogene 22 2003 8999 9006
9. J. Downward Ras signalling and apoptosis Curr. Opin. Genet. Dev. 8 1998 49 54
10. J. Downward, J.D. Graves, P.H. Warne, S. Rayter, and D.A. Cantrell Stimulation of p21ras upon T-cell activation Nature 346 1990 719 723
11. K. Eckfeld, L. Hesson, M.D. Vos, I. Bieche, F. Latif, and G.J. Clark RASSF4/AD037 is a potential ras effector/tumor suppressor of the RASSF family Cancer Res. 64 2004 8688 8693
12. M. Fivaz, and T. Meyer Reversible intracellular translocation of KRas but not HRas in hippocampal neurons regulated by Ca2+/calmodulin J. Cell Biol. 170 2005 429 441
13. J.S. Goodwin, K.R. Drake, C. Rogers, L. Wright, J. Lippincott-Schwartz, M.R. Philips, and A.K. Kenworthy Depalmitoylated Ras traffics to and from the Golgi complex via a nonvesicular pathway J. Cell Biol. 170 2005 261 272
14. ras to the plasma membrane Cell 63 1990 133 139
15. J.H. Jackson, J.W. Li, J.E. Buss, C.J. Der, and C.G. Cochrane Polylysine domain of K-ras 4B protein is crucial for malignant transformation Proc. Natl. Acad. Sci. USA 91 1994 12730 12734
16. A. Khokhlatchev, S. Rabizadeh, R. Xavier, M. Nedwidek, T. Chen, X.F. Zhang, B. Seed, and J. Avruch Identification of a novel Ras-regulated proapoptotic pathway Curr. Biol. 12 2002 253 265
17. J. Kortmansky, and G.K. Schwartz Bryostatin-1: a novel PKC inhibitor in clinical development Cancer Invest. 21 2003 924 936
18. M. Krajewska, S.F. Moss, S. Krajewski, K. Song, P.R. Holt, and J.C. Reed Elevated expression of Bcl-X and reduced Bak in primary colorectal adenocarcinomas Cancer Res. 56 1996 2422 2427
19. T. Kuwana, and D.D. Newmeyer Bcl-2-family proteins and the role of mitochondria in apoptosis Curr. Opin. Cell Biol. 15 2003 691 699
20. P. Lang, F. Gesbert, M. Delespine-Carmagnat, R. Stancou, M. Pouchelet, and J. Bertoglio Protein kinase A phosphorylation of RhoA mediates the morphological and functional effects of cyclic AMP in cytotoxic lymphocytes EMBO J. 15 1996 510 519
21. I. Lerosey, V. Pizon, A. Tavitian, and J. de Gunzburg The cAMP-dependent protein kinase phosphorylates the rap1 protein in vitro as well as in intact fibroblasts, but not the closely related rap2 protein Biochem. Biophys. Res. Commun. 175 1991 430 436
22. R. Leventis, and J.R. Silvius Lipid-binding characteristics of the polybasic carboxy-terminal sequence of K-ras4B Biochemistry 37 1998 7640 7648
23. B. Lin, S.K. Kolluri, F. Lin, W. Liu, Y.H. Han, X. Cao, M.I. Dawson, J.C. Reed, and X.K. Zhang Conversion of Bcl-2 from protector to killer by interaction with nuclear orphan receptor Nur77/TR3 Cell 116 2004 527 540
24. W. Liou, H.J. Geuze, and J.W. Slot Improving structural integrity of cryosections for immunogold labeling Histochem. Cell Biol. 106 1996 41 58
25. A.I. Magee, L. Gutierrez, I.A. McKay, C.J. Marshall, and A. Hall Dynamic fatty acylation of p21N-ras EMBO J. 6 1987 3353 3357
26. B.K. McIlroy, J.D. Walters, P.J. Blackshear, and J.D. Johnson Phosphorylation-dependent binding of a synthetic MARCKS peptide to calmodulin J. Biol. Chem. 266 1991 4959 4964
27. S. McLaughlin, and A. Aderem The myristoyl-electrostatic switch: a modulator of reversible protein-membrane interactions Trends Biochem. Sci. 20 1995 272 276
28. D. Michaelson, J. Silletti, G. Murphy, P. D'Eustachio, M. Rush, and M.R. Philips Differential localization of Rho GTPases in live cells. Regulation by hypervariable regions and RhoGDI binding J. Cell Biol. 152 2001 111 126
29. D. Michaelson, W. Ali, V.K. Chiu, M. Bergo, J. Silletti, L. Wright, S.G. Young, and M. Philips Postprenylation CAAX processing is required for proper localization of Ras but not Rho GTPases Mol. Biol. Cell 16 2005 1606 1616
30. L.A. Quilliam, H. Mueller, B.P. Bohl, V. Prossnitz, L.A. Sklar, C.J. Der, and G.M. Bokoch Rap1A is a substrate for cyclic AMP-dependent protein kinase in human neutrophils J. Immunol. 147 1991 1628 1635
31. A. Rebollo, D. Perez-Sala, and A.C. Martinez Bcl-2 differentially targets K-, N-, and H-Ras to mitochondria in IL-2 supplemented or deprived cells: implications in prevention of apoptosis Oncogene 18 1999 4930 4939
32. O. Rocks, A. Peyker, M. Kahms, P.J. Verveer, C. Koerner, M. Lumbierres, J. Kuhlmann, H. Waldmann, A. Wittinghofer, and P.I. Bastiaens An acylation cycle regulates localization and activity of palmitoylated Ras isoforms Science 307 2005 1746 1752
33. M.O. Roy, R. Leventis, and J.R. Silvius Mutational and biochemical analysis of plasma membrane targeting mediated by the farnesylated, polybasic carboxy terminus of K-ras4B Biochemistry 39 2000 8298 8307
34. L. Scorrano, S.A. Oakes, J.T. Opferman, E.H. Cheng, M.D. Sorcinelli, T. Pozzan, and S.J. Korsmeyer BAX and BAK regulation of endoplasmic reticulum Ca2+: a control point for apoptosis Science 300 2003 135 139
35. M.C. Seabra, and C. Wasmeier Controlling the location and activation of Rab GTPases Curr. Opin. Cell Biol. 16 2004 451 457
36. R.S. Sidhu, R.R. Clough, and R.P. Bhullar Ca2+/calmodulin binds and dissociates K-RasB from membrane Biochem. Biophys. Res. Commun. 304 2003 655 660
37. J.W. Slot, and H.J. Geuze A new method of preparing gold probes for multiple-labeling cytochemistry Eur. J. Cell Biol. 38 1985 87 93
38. J.W. Slot, H.J. Geuze, S. Gigengack, G.E. Lienhard, and D.E. James Immuno-localization of the insulin regulatable glucose transporter in brown adipose tissue of the rat J. Cell Biol. 113 1991 123 135
39. Z. Szallasi, C.B. Smith, G.R. Pettit, and P.M. Blumberg Differential regulation of protein kinase C isozymes by bryostatin 1 and phorbol 12-myristate 13-acetate in NIH 3T3 fibroblasts J. Biol. Chem. 269 1994 2118 2124
40. E.J. Uhlmann, T. Subramanian, C.A. Vater, R. Lutz, and G. Chinnadurai A potent cell death activity associated with transient high level expression of BCL-2 J. Biol. Chem. 273 1998 17926 17932
41. V.E. Valge, J.G. Wong, B.M. Datlof, A.J. Sinskey, and A. Rao Protein kinase C is required for responses to T cell receptor ligands but not to interleukin-2 in T cells Cell 55 1988 101 112
42. P. Villalonga, C. Lopez-Alcala, M. Bosch, A. Chiloeches, N. Rocamora, J. Gil, R. Marais, C.J. Marshall, O. Bachs, and N. Agell Calmodulin binds to K-Ras, but not to H- or N-Ras, and modulates its downstream signaling Mol. Cell. Biol. 21 2001 7345 7354
43. M.D. Vos, C.A. Ellis, C. Elam, A.S. Ulku, B.J. Taylor, and G.J. Clark RASSF2 is a novel K-Ras specific effector and potential tumor suppressor J. Biol. Chem. 278 2003 28045 28051
44. M.D. Vos, A. Martinez, C.A. Ellis, T. Vallecorsa, and G.J. Clark The Pro-apoptotic Ras effector Nore1 may serve as a Ras-regulated tumor suppressor in the lung J. Biol. Chem. 278 2003 21938 21943
45. N.S. Wang, M.T. Unkila, E.Z. Reineks, and C.W. Distelhorst Transient expression of wild-type or mitochondrially targeted Bcl-2 induces apoptosis, whereas transient expression of endoplasmic reticulum-targeted Bcl-2 is protective against Bax-induced cell death J. Biol. Chem. 276 2001 44117 44128