Copper is required for oncogenic BRAF signalling and tumorigenesis

Nature

Volumn 509, Issue 7501, 2014, Pages 492-496

  Brady, Donita C ^a   Crowe, Matthew S ^a   Turski, Michelle L ^a   Hobbs, G Aaron ^b   Yao, Xiaojie ^a   Chaikuad, Apirat ^c   Knapp, Stefan ^c   Xiao, Kunhong ^a   Campbell, Sharon L ^b   Thiele, Dennis J ^a   Counter, Christopher M ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

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

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

B RAF KINASE; COPPER; COPPER TRANSPORTER 1; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; UNCLASSIFIED DRUG;

CANCER; CHELATION; COPPER; DISEASE TREATMENT; GROWTH; INHIBITION; MUTATION; PUBLIC HEALTH; RODENT; TUMOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; GENE MUTATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TUMOR GROWTH;

ANIMALS; CATION TRANSPORT PROTEINS; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; CHELATING AGENTS; COPPER; DISEASE MODELS, ANIMAL; DRUG REPOSITIONING; DRUG RESISTANCE, NEOPLASM; FEMALE; HEPATOLENTICULAR DEGENERATION; HUMANS; INDOLES; LUNG NEOPLASMS; MAP KINASE SIGNALING SYSTEM; MICE; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS B-RAF; SULFONAMIDES; SURVIVAL ANALYSIS;

EID: 84901284074     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature13180     Document Type: Article

References (42)

1. Davies, H. et al. Mutations of the BRAF gene in human cancer. Nature 417, 949-954 (2002).
2. Forbes, S. A. et al. COSMIC: mining complete cancer genomes in the Catalogue of Somatic Mutations in Cancer. Nucleic Acids Res. 39, D945-D950 (2011).
3. Wan, P. T. et al. Mechanism of activation of the RAF-ERK signaling pathway by oncogenic mutations of B-RAF. Cell 116, 855-867 (2004).
4. Flaherty, K. T. et al. Improved survival with MEK inhibition in BRAF-mutated melanoma. N. Engl. J. Med. 367, 107-114 (2012).
5. Flaherty, K. T. et al. Combined BRAF and MEK inhibition in melanoma with BRAF V600 mutations. N. Engl. J. Med. 367, 1694-1703 (2012).
6. Turski, M. L. et al. A novel role for copper in Ras/mitogen-activated protein kinase signaling. Mol. Cell. Biol. 32, 1284-1295 (2012).
7. Ala, A., Walker, A. P., Ashkan, K., Dooley, J. S. & Schilsky, M. L. Wilson's disease. Lancet 369, 397-408 (2007).
8. Solit, D. B. et al. BRAF mutation predicts sensitivity to MEK inhibition. Nature 439, 358-362 (2006).
9. Lee, J., Petris, M. J. & Thiele, D. J. Characterization of mouse embryonic cells deficient in the ctr1 high affinity copper transporter. Identification of a Ctr1-independent copper transport system. J. Biol. Chem. 277, 40253-40259 (2002).
10. Bertinato, J. & L'Abbe, M. R. Copper modulates the degradation of copper chaperone for Cu,Zn superoxide dismutase by the 26S proteosome. J. Biol. Chem. 278, 35071-35078 (2003).
11. Puig, S., Lee, J., Lau, M.& Thiele, D. J. Biochemical and genetic analyses of yeast and human high affinity copper transporters suggest a conserved mechanism for copper uptake. J. Biol. Chem. 277, 26021-26030 (2002).
12. Bridgewater, J. D., Lim, J. & Vachet, R. W. Usingmetal-catalyzed oxidation reactions andmass spectrometry to identify amino acid residues within 10A? of the metal in Cu-binding proteins. J. Am. Soc. Mass Spectrom. 17, 1552-1559 (2006).
13. Fischmann, T. O. et al. Crystal structures of MEK1 binary and ternary complexes with nucleotides and inhibitors. Biochemistry 48, 2661-2674 (2009).
14. Huang, W., Kessler, D. S. & Erikson, R. L. Biochemical and biological analysis of Mek1 phosphorylation site mutants. Mol. Biol. Cell 6, 237-245 (1995).
15. Nakamura, K., Uhlik, M. T., Johnson, N. L., Hahn, K. M. & Johnson, G. L.PB1 domaindependent signaling complex is required for extracellular signal-regulated kinase 5 activation. Mol. Cell. Biol. 26, 2065-2079 (2006).
16. English, J. M. et al. Contribution of the ERK5/MEK5 pathway to Ras/Raf signaling and growth control. J. Biol. Chem. 274, 31588-31592 (1999).
17. Roberts, P. J. & Der, C. J. Targeting the Raf-MEK-ERK mitogen-activated protein kinase cascade for the treatment of cancer. Oncogene 26, 3291-3310 (2007).
18. Levin-Salomon, V., Kogan, K., Ahn, N. G., Livnah, O. & Engelberg, D. Isolation of intrinsically active (MEK-independent) variants of the ERK family of mitogen-activated protein (MAP) kinases. J. Biol. Chem. 283, 34500-34510 (2008).
19. Chu, Y., Solski, P. A., Khosravi-Far, R., Der, C. J. & Kelly, K. The mitogen-activated protein kinase phosphatases PAC1, MKP-1, and MKP-2 have unique substrate specificities and reduced activity in vivo toward the ERK2 sevenmaker mutation. J. Biol. Chem. 271, 6497-6501 (1996).
20. Turski, M. L. & Thiele, D. J. New roles for copper metabolism in cell proliferation, signaling, and disease. J. Biol. Chem. 284, 717-721 (2009).
21. Tsai, C. Y., Finley, J. C., Ali, S. S., Patel, H. H. & Howell, S. B. Copper influx transporter 1 is required for FGF, PDGF and EGF-induced MAPK signaling. Biochem. Pharmacol. 84, 1007-1013 (2012).
22. Nose, Y., Kim, B. E. & Thiele, D. J. Ctr1 drives intestinal copper absorption and is essential for growth, iron metabolism, and neonatal cardiac function. Cell Metab. 4, 235-244 (2006).
23. Dankort, D. et al. A new mouse model to explore the initiation, progression, and therapy of BRAFV600E-induced lung tumors. Genes Dev. 21, 379-384 (2007).
24. Solit, D. B. & Rosen, N. Resistance toBRAF inhibition in melanomas. N. Engl. J.Med. 364, 772-774 (2011).
25. Wagle, N. et al. Dissecting therapeutic resistance to RAF inhibition inmelanoma by tumor genomic profiling. J. Clin. Oncol. 29, 3085-3096 (2011).
26. Bridgewater, J. D. & Vachet, R. W. Metal-catalyzed oxidation reactions and mass spectrometry: the roles of ascorbate and different oxidizing agents in determining Cu-protein-binding sites. Anal. Biochem. 341, 122-130 (2005).
27. Kelly, S. M., Jess, T. J. & Price, N. C. How to study proteins by circular dichroism. Biochim. Biophys. Acta 1751, 119-139 (2005).
28. Niesen, F. H., Berglund, H.& Vedadi, M. The use of differential scanning fluorimetry to detect ligand interactions that promote protein stability. Nature Protocols 2, 2212-2221 (2007).
29. Augustine, C. K. et al. Sorafenib, a multikinase inhibitor, enhances the response of melanoma to regional chemotherapy. Mol. Cancer Ther. 9, 2090-2101 (2010).
30. Lampson, B. L. et al. Targeting eNOS in pancreatic cancer. Cancer Res. 72, 4472-4482 (2012).
31. O'Hayer, K. M. & Counter, C. M. A genetically defined normal human somatic cell system to study Ras oncogenesis in vivo and in vitro. Methods Enzymol. 407, 637-647 (2006).
32. Boehm, J. S. et al. Integrative genomic approaches identify IKBKE as a breast cancer oncogene. Cell 129, 1065-1079 (2007).
33. O'Hayer, K. M., Brady, D. C. & Counter, C. M. ELR1CXC chemokines and oncogenic Ras-mediated tumorigenesis. Carcinogenesis 30, 1841-1847 (2009).
34. Zipfel, P. A. et al. Ral activation promotes melanomagenesis. Oncogene 29, 4859-4864 (2010).
35. Scholl, F. A., Dumesic, P. A. & Khavari, P. A. Mek1 alters epidermal growth and differentiation. Cancer Res. 64, 6035-6040 (2004).
36. Johannessen, C. M. et al. COT drives resistance to RAF inhibition through MAP kinase pathway reactivation. Nature 468, 968-972 (2010).
37. Bric, A. et al. Functional identification of tumor-suppressor genes throughan in vivo RNA interference screen in a mouse lymphoma model. Cancer Cell 16, 324-335 (2009).
38. Kahsai, A. W. et al. Multiple ligand-specific conformations of the b2-adrenergic receptor. Nature Chem. Biol. 7, 692-700 (2011).
39. Nobles, K. N. et al. Distinct phosphorylation sites on the b2-adrenergic receptor establish a barcode that encodes differential functions of beta-arrestin. Sci. Signal. 4, ra51 (2011).
40. Rappsilber, J., Ishihama, Y. & Mann, M. Stop and go extraction tips for matrix-assisted laser desorption/ionization,nanoelectrospray, andLC/MSsample pretreatment in proteomics. Anal. Chem. 75, 663-670 (2003).
41. Haas, W. et al. Optimization and use of peptide mass measurement accuracy in shotgun proteomics. Mol. Cell. Proteomics 5, 1326-1337 (2006).
42. Hamad, N. M. et al. Distinct requirements for Ras oncogenesis in human versus mouse cells. Genes Dev. 16, 2045-2057 (2002).