A requirement for wild-type Ras isoforms in mutant KRas-driven signaling and transformation

Biochemical Journal

Volumn 452, Issue 2, 2013, Pages 313-320

  Bentley, Carolyn ^a   Jurinka, Stefanie S ^a   Kljavin, Noelyn M ^a   Vartanian, Steffan ^a   Ramani, Sree R ^a   Gonzalez, Lino C ^a   Yu, Kebing ^a   Modrusan, Zora ^a   Du, Pan ^a   Bourgon, Richard ^a   Neve, Richard M ^a   Stokoe, David ^a  

^a GENENTECH INC   (United States)

Author keywords

Akt; Extracellular signal regulated kinase (ERK); GTPase; Ras; Transformation; Zinc finger nuclease

Indexed keywords

K RAS PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; RAS PROTEIN;

ANCHORAGE INDEPENDENT GROWTH; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL MEMBRANE; CELL PROLIFERATION; CODING; COLONY FORMATION; ENDOMETRIUM CANCER; EXON; HUMAN; HUMAN CELL; IMMUNODETECTION; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; FEMALE; GTP PHOSPHOHYDROLASES; HUMANS; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; MICE, NUDE; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; PROTEIN ISOFORMS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS P21(RAS); RAS PROTEINS; SIGNAL TRANSDUCTION;

EID: 84877754445     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20121578     Document Type: Article

References (39)

1. Karnoub, A. and Weinberg, R. (2008) Ras oncogenes: split personalities. Nat. Rev. Mol. Cell Biol. 9, 517-531
2. Quinlan, M. P. and Settleman, J. (2009) Isoform-specific ras functions in development and cancer. Future Oncol. 5, 105-116
3. Augsten, M., Pusch, R., Biskup, C., Rennert, K., Wittig, U., Beyer, K., Blume, A., Wetzker, R., Friedrich, K. and Rubio, I. (2006) Live-cell imaging of endogenous Ras-GTP illustrates predominant Ras activation at the plasma membrane. EMBO Rep. 7, 46-51
4. Di Nicolantonio, F., Arena, S., Gallicchio, M., Zecchin, D., Martini, M., Flonta, S. E., Stella, G. M., Lamba, S., Cancelliere, C., Russo, M. et al. (2008) Replacement of normal with mutant alleles in the genome of normal human cells unveils mutation-specific drug responses. Proc. Natl. Acad. Sci. U.S.A. 105, 20864-20869
5. Rodriguez-Viciana, P., Sabatier, C. and McCormick, F. (2004) Signaling specificity by Ras family GTPases is determined by the full spectrum of effectors they regulate. Mol. Cell. Biol. 24, 4943-4954
6. Tuveson, D., Shaw, A., Willis, N., Silver, D., Jackson, E., Chang, S., Mercer, K., Grochow, R., Hock, H., Crowley, D. et al. (2004) Endogenous oncogenic K-ras(G12D) stimulates proliferation and widespread neoplastic and developmental defects. Cancer Cell 5, 375-387
7. Braun, B., Tuveson, D., Kong, N., Le, D., Kogan, S., Rozmus, J., Le Beau, M., Jacks, T. and Shannon, K. (2004) Somatic activation of oncogenic Kras in hematopoietic cells initiates a rapidly fatal myeloproliferative disorder. Proc. Natl. Acad. Sci. U.S.A. 101, 597-602
8. Konishi, H., Karakas, B., Abukhdeir, A. M., Lauring, J., Gustin, J. P., Garay, J. P., Konishi, Y., Gallmeier, E., Bachman, K. E. and Park, B. H. (2007) Knock-in of mutant K-ras in nontumorigenic human epithelial cells as a new model for studying K-ras mediated transformation. Cancer Res. 67, 8460-8467
9. Yan, J., Roy, S., Apolloni, A., Lane, A. and Hancock, J. (1998) Ras isoforms vary in their ability to activate Raf-1 and phosphoinositide 3-kinase. J Biol. Chem. 273, 24052-24056
10. Voice, J., Klemke, R., Le, A. and Jackson, J. (1999) Four human ras homologs differ in their abilities to activate Raf-1, induce transformation, and stimulate cell motility. J. Biol. Chem. 274, 17164-17170
11. Guerrero, I., Villasante, A., Corces, V. and Pellicer, A. (1985) Loss of the normal N-ras allele in a mouse thymic lymphoma induced by a chemical carcinogen. Proc. Natl. Acad. Sci. U.S.A. 82, 7810-7814
12. Bremner, R. and Balmain, A. (1990) Genetic changes in skin tumor progression: correlation between presence of a mutant ras gene and loss of heterozygosity on mouse chromosome 7. Cell 61, 407-417
13. Hegi, M. E., Devereux, T. R., Dietrich, W. F., Cochran, C. J., Lander, E. S., Foley, J. F., Maronpot, R. R., Anderson, M. W. and Wiseman, R. W. (1994) Allelotype analysis of mouse lung carcinomas reveals frequent allelic losses on chromosome 4 and an association between allelic imbalances on chromosome 6 and K-ras activation. Cancer Res. 54, 6257-6264
14. Zhang, Z., Wang, Y., Vikis, H., Johnson, L., Liu, G., Li, J., Anderson, M., Sills, R., Hong, H., Devereux, T. et al. (2001) Wildtype Kras2 can inhibit lung carcinogenesis in mice. Nat. Genet. 29, 25-33
15. Diaz, R., Ahn, D., Lopez-Barcons, L., Malumbres, M., Pérez de Castro, I., Lue, J., Ferrer-Miralles, N., Mangues, R., Tsong, J., Garcia, R. et al. (2002) The N-ras proto-oncogene can suppress the malignant phenotype in the presence or absence of its oncogene. Cancer Res. 62, 4514-4518
16. Junttila, M. R., Karnezis, A. N., Garcia, D., Madriles, F., Kortlever, R. M., Rostker, F., Brown-Swigart, L., Pham, D. M., Seo, Y., Evan, G. I. et al. (2010) Selective activation of p53-mediated tumour suppression in high-grade tumours. Nature 468, 567-571
17. Spandidos, D. A., Frame, M. and Wilkie, N. M. (1990) Expression of the normal H-ras1 gene can suppress the transformed and tumorigenic phenotypes induced by mutant ras genes. Anticancer Res. 10, 1543-1554
18. Diaz, R., Lue, J., Mathews, J., Yoon, A., Ahn, D., Garcia-España, A., Leonardi, P., Vargas, M. P. and Pellicer, A. (2005) Inhibition of Ras oncogenic activity by Ras protooncogenes. Int. J. Cancer 113, 241-248
19. Lim, K.-H., Ancrile, B. B., Kashatus, D. F. and Counter, C. M. (2008) Tumour maintenance is mediated by eNOS. Nature 452, 646-649
20. Boykevisch, S., Zhao, C., Sondermann, H., Philippidou, P., Halegoua, S., Kuriyan, J. and Bar-Sagi, D. (2006) Regulation of ras signaling dynamics by Sos-mediated positive feedback. Curr. Biol. 16, 2173-2179
21. Carroll, D. (2011) Genome engineering with zinc-finger nucleases. Genetics 188, 773-782
22. Davis, D. and Stokoe, D. (2010) Zinc finger nucleases as tools to understand and treat human diseases. BMC Med. 8, 42
23. Kim, J.-S., Lee, C., Foxworth, A. and Waldman, T. (2004) B-Raf is dispensable for K-Ras-mediated oncogenesis in human cancer cells. Cancer Res. 64, 1932-1937
24. Gerber, S. A., Rush, J., Stemman, O., Kirschner, M. W. and Gygi, S. P. (2003) Absolute quantification of proteins and phosphoproteins from cell lysates by tandem MS. Proc. Natl. Acad. Sci. U.S.A. 100, 6940-6945
25. Prabakaran, S., Everley, R. A., Landrieu, I., Wieruszeski, J.-M., Lippens, G., Steen, H. and Gunawardena, J. (2011) Comparative analysis of Erk phosphorylation suggests a mixed strategy for measuring phospho-form distributions. Mol. Syst. Biol. 7, 482
26. Vartanian, S., Bentley, C., Brauer, M. J., Li, L., Shirasawa, S., Sasazuki, T., Kim, J.-S., Haverty, P., Stawiski, E., Modrusan, Z. et al. (2013) Identification of mutant KRas-dependent phenotypes using a panel of isogenic cell lines. J. Biol. Chem. 288, 2403-2413
27. Vanhaesebroeck, B., Guillermet-Guibert, J., Graupera, M. and Bilanges, B. (2010) The emerging mechanisms of isoform-specific PI3K signalling. Nat. Rev. Mol. Cell Biol. 11, 329-341
28. Rodriguez-Viciana, P., Warne, P., Dhand, R., Vanhaesebroeck, B., Gout, I., Fry, M., Waterfield, M. and Downward, J. (1994) Phosphatidylinositol-3-OH kinase as a direct target of Ras. Nature 370, 527-532
29. Jorissen, R. N., Walker, F., Pouliot, N., Garrett, T. P. J., Ward, C. W. and Burgess, A. W. (2003) Epidermal growth factor receptor: mechanisms of activation and signalling. Exp. Cell Res. 284, 31-53
30. Ganguly, A., Wang, Y., Pramanik, B., Doll, R., Snow, M., Taveras, A., Remiszewski, S., Cesarz, D., del Rosario, J., Vibulbhan, B. et al. (1998) Interaction of a novel GDP exchange inhibitor with the Ras protein. Biochemistry 37, 15631-15637
31. Peri, F., Airoldi, C., Colombo, S., Mari, S., Jimenez-Barbero, J., Martegani, E. and Nicotra, F. (2006) Sugar-derived Ras inhibitors: group epitope mapping by NMR spectroscopy and biological function. Eur. J. Org. Chem. 2006, 3707-3720
32. Maurer, T., Garrenton, L. S., Oh, A., Pitts, K., Anderson, D. J., Skelton, N. J., Fauber, B. P., Pan, B., Malek, S., Stokoe, D. et al. (2012) Small-molecule ligands bind to a distinct pocket in Ras and inhibit SOS-mediated nucleotide exchange activity. Proc. Natl. Acad. Sci. U.S.A. 109, 5299-5304
33. Sun, Q., Burke, J. P., Phan, J., Burns, M. C., Olejniczak, E. T., Waterson, A. G., Lee, T., Rossanese, O. W. and Fesik, S. W. (2012) Discovery of small molecules that bind to K-Ras and inhibit Sos-mediated activation. Angew. Chem. Int. Ed. 51, 6140-6143
34. Stewart, S. and Guan, K. (2000) The dominant negative Ras mutant, N17Ras, can inhibit signaling independently of blocking Ras activation. J. Biol. Chem. 275, 8854-8862
35. Qian, X., Esteban, L., Vass, W., Upadhyaya, C., Papageorge, A., Yienger, K., Ward, J., Lowy, D. and Santos, E. (2000) The Sos1 and Sos2 Ras-specific exchange factors: differences in placental expression and signaling properties. EMBO J. 19, 642-654
36. Young, A., Lou, D. and McCormick, F. (2013) Oncogenic and wild-type Ras play divergent roles in the regulation of mitogen-activated protein kinase signaling. Cancer Discovery 3, 112-123
37. Jeng, H.-H., Taylor, L. J. and Bar-Sagi, D. (2012) Sos-mediated cross-activation of wild-type Ras by oncogenic Ras is essential for tumorigenesis. Nat. Commun. 3, 1168
38. Gabriel, R., Lombardo, A., Arens, A., Miller, J. C., Genovese, P., Kaeppel, C., Nowrouzi, A., Bartholomae, C. C., Wang, J., Friedman, G. et al. (2011) An unbiased genome-wide analysis of zinc-finger nuclease specificity. Nat. Biotechnol. 29, 816-823
39. Miller, J., Tan, S., Qiao, G., Barlow, K., Wang, J., Xia, D., Meng, X., Paschon, D., Leung, E., Hinkley, S. et al. (2011) A TALE nuclease architecture for efficient genome editing. Nat. Biotechnol. 29, 143-148