Metabolic dependencies in RAS-driven cancers

Clinical Cancer Research

Volumn 21, Issue 8, 2015, Pages 1828-1834

  Kimmelman, Alec C ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 (N ETHYL N ISOPROPYL)AMILORIDE; ASPARTATE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE ISOENZYME 2; CHLOROQUINE; CYTOSOLIC ASPARTATE AMINOTRANSFERASE; GLUTAMATE DEHYDROGENASE; HEXOSAMINE; HYDROXYCHLOROQUINE; MALATE DEHYDROGENASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE; RAF PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; UNCLASSIFIED DRUG; PROTEIN P21;

ADAPTATION; AEROBIC GLYCOLYSIS; ANTINEOPLASTIC ACTIVITY; ARTICLE; BIOSYNTHESIS; CANCER MODEL; CARCINOGENESIS; CELL PROLIFERATION; CITRIC ACID CYCLE; COLON ADENOCARCINOMA; DRUG EFFICACY; ENZYME REGULATION; GENE FREQUENCY; GENE FUNCTION; GENE MUTATION; GENETIC ASSOCIATION; GLUCOSE METABOLISM; GLYCOLYSIS; HUMAN; INTERNALIZATION; LUNG CANCER; MACROAUTOPHAGY; MALIGNANT NEOPLASTIC DISEASE; METABOLIC ADAPTATION; METABOLISM; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NONHUMAN; NUCLEAR REPROGRAMMING; ONCOGENE K RAS; ONCOGENE RAS; OXIDATION REDUCTION STATE; OXIDATIVE PHOSPHORYLATION; PANCREAS ADENOCARCINOMA; PANCREAS CANCER; PINOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TUMOR CELL; TUMOR GROWTH; TUMOR METABOLISM; TUMOR MICROENVIRONMENT; ANIMAL; CELL TRANSFORMATION; ENERGY METABOLISM; GENETICS; NEOPLASM; OXYGEN CONSUMPTION;

ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; ENERGY METABOLISM; HUMANS; METABOLIC NETWORKS AND PATHWAYS; NEOPLASMS; OXYGEN CONSUMPTION; PROTO-ONCOGENE PROTEINS P21(RAS);

EID: 84927632705     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-14-2425     Document Type: Article

References (70)

1. Cox AD, Fesik SW, Kimmelman AC, Luo J, Der CJ. Drugging the undruggable RAS: mission possible? Nat Rev Drug Discov 2014;13:828-51.
2. Stephen AG, Esposito D, Bagni RK, McCormick F. Dragging ras back in the ring. Cancer Cell 2014;25:272-81.
3. Pylayeva-Gupta Y, Grabocka E, Bar-Sagi D. RAS oncogenes: weaving a tumorigenic web. Nat Rev Cancer 2011;11:761-74.
4. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011;144:646-74.
5. Engelman JA, Chen L, Tan X, Crosby K, Guimaraes AR, Upadhyay R, et al. Effective use of PI3K and MEK inhibitors to treat mutant Kras G12D and PIK3CA H1047R murine lung cancers. Nat Med 2008;14:1351-6.
6. Alagesan B, Contino G, Guimaraes AR, Corcoran RB, Desphande V, Wojtkiewicz GR, et al. Combined MEK and PI3K inhibition in a mouse model of pancreatic cancer. Clin Cancer Res 2015;21:396-404.
7. Cox AD, Der CJ, Philips MR. Targeting RAS membrane association: back to the future for anti-Ras drug discovery? Clin Cancer Res 2015;21:1819-27.
8. Downward J. RAS synthetic lethal screens revisited: still seeking the elusive prize? Clin Cancer Res 2015;21:1802-9.
9. Marcus K, Mattos C. Direct attack on RAS: intramolecular communication and mutation-specific effects. Clin Cancer Res 2015;21:1810-8.
10. McCormick F. KRAS as a therapeutic target. Clin Cancer Res 2015;21: 1797-801.
11. Berardi MJ, Fantin VR. Survival of the fittest: metabolic adaptations in cancer. Curr Opin Genet Dev 2011;21:59-66.
12. Stine ZE, Dang CV. Stress eating and tuning out: cancer cells re-wire metabolism to counter stress. Crit Rev Biochem Mol Biol 2013;48:609-19.
13. Dang CV. Links between metabolism and cancer. Genes Dev 2012;26: 877-90.
14. Ward PS, Thompson CB. Metabolic reprogramming: a cancer hallmark even Warburg did not anticipate. Cancer Cell 2012;21:297-308.
15. Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: themetabolic requirements of cell proliferation. Science 2009; 324:1029-33.
16. Weinberg F, Hamanaka R, Wheaton WW, Weinberg S, Joseph J, Lopez M, et al. Mitochondrial metabolism and ROS generation are essential for Kras-mediated tumorigenicity. Proc Natl Acad Sci U S A 2010;107:8788-93.
17. Fan J, Kamphorst JJ, Mathew R, Chung MK, White E, Shlomi T, et al. Glutamine-driven oxidative phosphorylation is a major ATP source in transformed mammalian cells in both normoxia and hypoxia. Mol Syst Biol 2013;9:712.
18. Chandel NS. Navigating metabolism. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press; 2014.
19. Kimmelman AC. The dynamic nature of autophagy in cancer. Genes Dev 2011;25:1999-2010.
20. Yang Z, Klionsky DJ. Eaten alive: a history of macroautophagy. Nat Cell Biol 2010;12:814-22.
21. Levine B, Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008;132:27-42.
22. Kroemer G, Mariño G, Levine B. Autophagy and the integrated stress response. Mol Cell 2010;40:280-93.
23. Yang Z, Klionsky DJ. Mammalian autophagy: core molecular machinery and signaling regulation. Curr Opin Cell Biol 2010;22:124-131.
24. Rogov V, Dötsch V, Johansen T, Kirkin V. Interactions between autophagy receptors and ubiquitin-like proteins form themolecular basis for selective autophagy. Mol Cell 2014;53:167-78.
25. Schreiber A, Peter M. Substrate recognition in selective autophagy and the ubiquitin-proteasome system. Biochim Biophys Acta 2014;1843:163-81.
26. Shaid S, Brandts CH, Serve H, Dikic I. Ubiquitination and selective autophagy. Cell Death Differ 2013;20:21-30.
27. Rabinowitz JD, White E. Autophagy and metabolism. Science 2010;330: 1344-8.
28. Mancias JD, Wang X, Gygi SP, Harper JW, Kimmelman AC. Quantitative proteomics identi fies NCOA4 as the cargo receptor mediating ferritinophagy. Nature 2014;509:105-9.
29. Yang S, Wang X, Contino G, Liesa M, Sahin E, Ying H, et al. Pancreatic cancers require autophagy for tumor growth. Genes Dev 2011;25:717-29.
30. Lock R, Roy S, Kenific CM, Su JS, Salas E, Ronen SM, et al. Autophagy facilitates glycolysis during Ras-mediated oncogenic transformation. Mol Biol Cell 2011;22:165-78.
31. Guo JY, Chen HY, Mathew R, Fan J, Strohecker AM, Karsli-Uzunbas G, et al. Activated Ras requires autophagy to maintain oxidative metabolism and tumorigenesis. Genes Dev 2011;25:460-70.
32. Kim MJ, Woo SJ, Yoon CH, Lee JS, An S, Choi YH, et al. Involvement of autophagy in oncogenic K-Ras-induced malignant cell transformation. J Biol Chem 2011;286:12924-32.
33. Guo JY, Karsli-Uzunbas G, Mathew R, Aisner SC, Kamphorst JJ, Strohecker AM, et al. Autophagy suppresses progression of K-ras-induced lung tumors to oncocytomas and maintains lipid homeostasis. Genes Dev 2013;27: 1447-61.
34. Karsli-Uzunbas G, Guo JY, Price S, Teng X, Laddha SV, Khor S, et al. Autophagy is required for glucose homeostasis and lung tumor maintenance. Cancer Discov 2014;4:914-27.
35. Yang A, Rajeshkumar NV, Wang X, Yabuuchi S, Alexander BM, Chu GC, et al. Autophagy is critical for pancreatic tumor growth and progression in tumors with p53 alterations. Cancer Discov 2014;4:905-13.
36. Yang A, Kimmelman AC. Inhibition of autophagy attenuates pancreatic cancer growth independent of TP53/TRP53 status. Autophagy 2014;10: 1683-4.
37. Rosenfeldt MT, O'Prey J, Morton JP, Nixon C, MacKay G, Mrowinska A, et al. p53 status determines the role of autophagy in pancreatic tumour development. Nature 2013;504:296-300.
38. Rosenfeld MR, Ye X, Supko JG, Desideri S, Grossman SA, Brem S, et al. A phase I/II trial of hydroxychloroquine in conjunction with radiation therapy and concurrent and adjuvant temozolomide in patients with newly diagnosed glioblastoma multiforme. Autophagy 2014;10: 1359-68.
39. Rangwala R, Leone R, Chang YC, Fecher LA, Schuchter LM, Kramer A, et al. Combined MTOR and autophagy inhibition: phase I trial of hydroxychloroquine and temsirolimus in patients with advanced solid tumors and melanoma. Autophagy 2014;10:1391-402.
40. Barnard RA, Wittenburg LA, Amaravadi RK, Gustafson DL, Thorburn A, Thamm DH. Phase I clinical trial and pharmacodynamic evaluation of combination hydroxychloroquine and doxorubicin treatment in pet dogs treated for spontaneously occurring lymphoma. Autophagy 2014;10: 1415-25.
41. Mahalingam D, Mita M, Sarantopoulos J, Wood L, Amaravadi RK, Davis LE, et al. Combined autophagy and HDAC inhibition: a phase I safety, tolerability, pharmacokinetic, and pharmacodynamic analysis of hydroxychloroquine in combination with the HDAC inhibitor vorinostat in patients with advanced solid tumors. Autophagy 2014;10:1403-14.
42. Vogl DT, Stadtmauer EA, Tan KS, Heitjan DF, Davis LE, Pontiggia L, et al. Combined autophagy and proteasome inhibition: a phase 1 trial of hydroxychloroquine and bortezomib in patients with relapsed/refractory myeloma. Autophagy 2014;10:1380-90.
43. Wolpin BM, Rubinson DA, Wang X, Chan JA, Cleary JM, Enzinger PC, et al. Phase II and pharmacodynamic study of autophagy inhibition using hydroxychloroquine in patients with metastatic pancreatic adenocarcinoma. Oncologist 2014;19:637-8.
44. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012;8:445-544.
45. Amaravadi RK, Lippincott-Schwartz J, Yin XM, Weiss WA, Takebe N, Timmer W, et al. Principles and current strategies for targeting autophagy for cancer treatment. Clin Cancer Res 2011;17:654-66.
46. Carmichael SJ, Charles B, Tett SE. Population pharmacokinetics of hydroxychloroquine in patients with rheumatoid arthritis. Ther Drug Monit 2003;25:671-81.
47. nd edition). Autophagy 2011;7:1273-94.
48. Bar-Sagi D, Feramisco JR. Induction of membrane ruffling and fluid-phase pinocytosis in quiescent fibroblasts by Ras proteins. Science 1986;233: 1061-8.
49. Swanson JA, Watts C. Macropinocytosis. Trends Cell Biol 1995;5:424-8.
50. Lim JP, Gleeson PA. Macropinocytosis: an endocytic pathway for internalising large gulps. Immunol Cell Biol 2011;89:836-43.
51. Commisso C, Davidson SM, Soydaner-Azeloglu RG, Parker SJ, Kamphorst JJ, Hackett S, et al. Macropinocytosis of protein is an amino acid supply route in Ras-transformed cells. Nature 2013;497:633-7.
52. Koivusalo M, Welch C, Hayashi H, Scott CC, Kim M, Alexander T, et al. Amiloride inhibits macropinocytosis by lowering submembranous pH and preventing Rac1 and Cdc42 signaling. J Cell Biol 2010;188:547-63.
53. Kamphorst JJ, Cross JR, Fan J, de Stanchina E, Mathew R, White EP, et al. Hypoxic and Ras-transformed cells support growth by scavenging unsaturated fatty acids from lysophospholipids. Proc Natl Acad Sci U S A 2013;110:8882-7.
54. Von Hoff DD, Ervin T, Arena FP, Chiorean EG, Infante J, Moore M, et al. Increased survival in pancreatic cancer with nab-paclitaxel plus gemcitabine. N Engl J Med 2013;369:1691-703.
55. Ying H, Kimmelman AC, Lyssiotis CA, Hua S, Chu GC, Fletcher-Sananikone E, et al. Oncogenic Kras maintains pancreatic tumors through regulation of anabolic glucose metabolism. Cell 2012;149:656-70.
56. Collins MA, Bednar F, Zhang Y, Brisset JC, Galbán S, Galbán CJ, et al. Oncogenic Kras is required for both the initiation and maintenance of pancreatic cancer in mice. J Clin Invest 2012;122:639-53.
57. Son J, Lyssiotis CA, Ying H, Wang X, Hua S, Ligorio M, et al. Glutamine supports pancreatic cancer growth through a KRAS-regulated metabolic pathway. Nature 2013;496:101-5.
58. Lyssiotis CA, Son J, Cantley LC, Kimmelman AC. Pancreatic cancers rely on a novel glutamine metabolism pathway to maintain redox balance. Cell Cycle 2013;12:1987-8.
59. Gaglio D, Metallo CM, Gameiro PA, Hiller K, Danna LS, Balestrieri C, et al. Oncogenic K-Ras decouples glucose and glutamine metabolism to support cancer cell growth. Mol Syst Biol 2011;7:523.
60. Dall'Olio F, Malagolini N, Trinchera M, Chiricolo M. Mechanisms of cancer-associated glycosylation changes. Front Biosci 2012;17:670-99.
61. DeNicola GM, Karreth FA, Humpton TJ, Gopinathan A, Wei C, Frese K, et al. Oncogene-induced Nrf2 transcription promotes ROS detoxification and tumorigenesis. Nature 2011;475:106-9.
62. Shelton P, Jaiswal AK. The transcription factor NF-E2-related factor 2 (Nrf2): a protooncogene? FASEB J 2013;27:414-23.
63. Jaramillo MC, Zhang DD. The emerging role of the Nrf2-Keap1 signaling pathway in cancer. Genes Dev 2013;27:2179-91.
64. Mitsuishi Y, Taguchi K, Kawatani Y, Shibata T, Nukiwa T, Aburatani H, et al. Nrf2 redirects glucose and glutamine into anabolic pathways in metabolic reprogramming. Cancer Cell 2012; 22:66-79.
65. Zhao Y, Adjei AA. The clinical development of MEK inhibitors. Nat Rev Clin Oncol 2014;11:385-400.
66. Gross MI, Demo SD, Dennison JB, Chen L, Chernov-Rogan T, Goyal B, et al. Antitumor activity of the glutaminase inhibitor CB-839 in triple-negative breast cancer. Mol Cancer Ther 2014;13:890-901.
67. Berkers CR, Maddocks OD, Cheung EC, Mor I, Vousden KH. Metabolic regulation by p53 family members. Cell Metab 2013;18:617-33.
68. Vousden KH, Ryan KM. p53 and metabolism. Nat Rev Cancer 2009;9: 691-700.
69. Levine AJ, Puzio-Kuter AM. The control of the metabolic switch in cancers by oncogenes and tumor suppressor genes. Science 2010;330:1340-4.
70. Viale A, Pettazzoni P, Lyssiotis CA, Ying H, Sánchez N, Marchesini M, et al. Oncogene ablation-resistant pancreatic cancer cells depend on mitochondrial function. Nature 2014;514:628-32.