Aspartate rescues S-phase arrest caused by suppression of glutamine utilization in KRas-driven cancer cells

Journal of Biological Chemistry

Volumn 291, Issue 17, 2016, Pages 9322-9329

  Patel, Deven ^a,b   Menon, Deepak ^a,b   Bernfeld, Elyssa ^a,b   Mroz, Victoria ^a   Kalan, Sampada ^a,b   Loayza, Diego ^a,b   Foster, David A ^a,b,c  

^a CITY UNIVERSITY OF NEW YORK   (United States)

^b CITY UNIVERSITY OF NEW YORK   (United States)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BIOCHEMISTRY; BIOSYNTHESIS; CARBON; CYTOLOGY; DISEASES; METABOLITES; NUCLEOTIDES;

ATAXIA TELANGIECTASIA; DAUGHTER CELLS; DNA SYNTHESISS; GROWTH FACTOR; KETOGLUTARATE; MOLECULAR BASIS; NITROGEN SOURCES; NUCLEOTIDE BIOSYNTHESIS;

CELLS;

2 OXOGLUTARIC ACID; AMINOTRANSFERASE; ASPARTIC ACID; ATR PROTEIN; DEOXYRIBONUCLEOTIDE; GLUTAMIC ACID; GLUTAMINE; K RAS PROTEIN; OXALOACETIC ACID; ATM PROTEIN; ATR PROTEIN, HUMAN; KRAS PROTEIN, HUMAN; PROTEIN P21; PURINE NUCLEOTIDE; PYRIMIDINE NUCLEOTIDE;

AMINO ACID METABOLISM; ARTICLE; CANCER CELL; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVATION; ENZYME MECHANISM; HUMAN; HUMAN CELL; METABOLITE; PRIORITY JOURNAL; S PHASE CELL CYCLE CHECKPOINT; BIOSYNTHESIS; CITRIC ACID CYCLE; G1 PHASE CELL CYCLE CHECKPOINT; GENETICS; MCF-7 CELL LINE; METABOLISM;

ASPARTIC ACID; ATAXIA TELANGIECTASIA MUTATED PROTEINS; CITRIC ACID CYCLE; G1 PHASE CELL CYCLE CHECKPOINTS; GLUTAMIC ACID; HUMANS; MCF-7 CELLS; PROTO-ONCOGENE PROTEINS P21(RAS); PURINE NUCLEOTIDES; PYRIMIDINE NUCLEOTIDES; S PHASE CELL CYCLE CHECKPOINTS;

EID: 84965010266     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.710145     Document Type: Article

References (26)

1. Hanahan, D., and Weinberg, R. A. (2011) Hallmarks of cancer: the next generation. Cell 144, 646-674
2. Vander Heiden, M. G., Cantley, L. C., and Thompson, C. B. (2009) Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324, 1029-1033
3. DeBerardinis, R. J., Mancuso, A., Daikhin, E., Nissim, I., Yudkoff, M., Wehrli, S., and Thompson, C. B.(2007) Beyond aerobic glycolysis: transformed cells can engage in glutamine metabolism that exceeds the requirement for protein and nucleotide synthesis. Proc. Natl. Acad. Sci. U.S.A. 104, 19345-19350
4. Wise, D. R., and Thompson, C. B. (2010) Glutamine addiction: a new therapeutic target in cancer. Trends Biochem. Sci. 35, 427-433
5. Zhang, J., Fan, J., Venneti, S., Cross, J. R., Takagi, T., Bhinder, B., Djaballah, H., Kanai, M., Cheng, E. H., Judkins, A. R., Pawel, B., Baggs, J., Cherry, S., Rabinowitz, J. D., and Thompson, C. B. (2014) Asparagine plays a critical role in regulating cellular adaptation to glutamine depletion. Mol Cell 56, 205-218
6. Foster, D. A., Yellen, P., Xu, L., and Saqcena, M. (2010) Regulation of G1 Cell Cycle Progression: Distinguishing the Restriction Point from a Nutrient-Sensing Cell Growth Checkpoint(s). Genes Cancer 1, 1124-1131
7. Wise, D. R., and DeBerardinis., R. J., Mancuso, A., Sayed, N., Zhang, X. Y., Pfeiffer, H. K., Nissim, I., Daikhin, E., Yudkoff, M., McMahon, S. B., and Thompson, C. B. (2008) Myc regulates a transcriptional program that stimulates mitochondrial glutaminolysis and leads toglutamine addiction. Proc. Natl. Acad. Sci. U.S.A. 105, 18782-18787
8. Yuneva, M., Zamboni, N., Oefner, P., Sachidanandam, R., and Lazebnik, Y. (2007) Deficiency in glutamine but not glucose induces MYC-dependent apoptosis in human cells. J. Cell Biol. 178, 93-105
9. Saqcena, M., Menon, D., Patel, D., Mukhopadhyay, S., Chow, V., and Foster, D. A. (2013) Amino acids and mTOR mediate distinct metabolic checkpoints in mammalian G1 cell cycle. PLoS ONE 8, e74157
10. Goodarzi, A. A., and Block., W. D., and Lees-Miller, S. P. (2003) The role of ATM and ATR in DNA damage-induced cell cycle control. Prog Cell Cycle Res 5, 393-411
11. Gaillard, H., García-Muse, T., and Aguilera, A. (2015) Replication stress and cancer. Nat. Rev. Cancer 15, 276-289
12. Saqcena, M., Mukhopadhyay, S., Hosny, C., Alhamed, A., Chatterjee, A., and Foster, D. A. (2015) Blocking anaplerotic entry of glutamine into the TCA cycle sensitizes K-Ras mutant cancer cells to cytotoxic drugs. Oncogene 34, 2672-2680
13. Saqcena, M., Patel, D., Menon, D., Mukhopadhyay, S., and Foster, D. A. (2015) Apoptotic effects of high-dose rapamycin occur in S-phase of the cell cycle. Cell Cycle 14, 2285-2292
14. Wasa, M., and Bode., B. P., Abcouwer, S. F., Collins, C. L., Tanabe, K. K., and Souba, W. W. (1996) Glutamine as a regulator of DNA and protein biosynthesis in human solid tumor cell lines. Ann. Surg. 224, 189-197
15. Boza, J. J., Moennoz, D., Bournot, C. E., Blum, S., Zbinden, I., and Finot., P. A., and Ballevre, O.(2000) Roleofglutamine on the de novo purine nucleotide synthesis in Caco-2 cells. Eur. J. Nutrition 39, 38-46
16. Son, J., and Lyssiotis., C. A., Ying, H., Wang, X., Hua, S., Ligorio, M., Perera, R. M., Ferrone, C.R., Mullarky, E., Shyh-Chang, N., Kang, Y., Fleming, J.B., Bardeesy, N., Asara, J.M., Haigis, M. C., DePinho, R.A., Cantley, L. C., and Kimmelman, A. C. (2013) Glutamine supports pancreatic cancer growth through a KRAS-regulated metabolic pathway. Nature 496, 101-105
17. Abraham, R. T. (2001) Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 15, 2177-2196
18. Brown, E. J., and Baltimore, D. (2003) Essential and dispensable roles of ATR in cell cycle arrest and genome maintenance. Genes Dev. 17, 615-628
19. Reinhardt, H. C., and Yaffe, M. B. (2009) Kinases that control the cell cycle in response to DNA damage: Chk1, Chk2, and MK2. Curr. Opin. Cell Biol. 21, 245-255
20. Dai, Y., Chen, S., Kmieciak, M., Zhou, L., Lin, H., Pei, X. Y., and Grant, S. (2013) The novel Chk1 inhibitor MK-8776 sensitizes human leukemia cells to HDAC inhibitors by targeting the intra-S checkpoint and DNA replication and repair. Mol. Cancer Ther. 12, 878-889
21. Cox, A. D., and Fesik., S. W., Kimmelman, A. C., Luo, J., and Der, C. J. (2014) Drugging the undruggable RAS: Mission possible? Nat. Rev. Drug Discov. 13, 828-851
22. Van Vranken, J. G., and Rutter, J. (2015) You Down With ETC? Yeah, You Know D¡ Cell 162, 471-473
23. Schoors, S., Bruning, U., Missiaen, R., Queiroz, K. C., Borgers, G., Elia, I., Zecchin, A., Cantelmo, A. R., Christen, S., Goveia, J., Heggermont, W., Goddé, L., Vinckier, S., Van Veldhoven, P. P., Eelen, G., Schoonjans, L., Gerhardt, H., Dewerchin, M., Baes, M., De Bock, K., Ghesquière, B., Lunt, S. Y., Fendt, S. M., and Carmeliet, P. (2015) Fatty acid carbon is essential for dNTP synthesis in endothelial cells. Nature 520, 192-197
24. Rabinovich, S., Adler, L., Yizhak, K., Sarver, A., Silberman, A., Agron, S., Stettner, N., Sun, Q., Brandis, A., Helbling, D., Korman, S., Itzkovitz, S., Dimmock, D., Ulitsky, I., Nagamani, S. C., Ruppin, E., and Erez, A. (2015) Diversion of aspartate in ASS1-deficient tumours fosters de novo pyrimidine synthesis. Nature 527, 379-383
25. Sullivan, L. B., and Gui., D. Y., Hosios, A. M., Bush, L. N., Freinkman, E., and Vander Heiden, M. G. (2015) Supporting aspartate biosynthesis is an essential function of respiration in proliferating cells. Cell 162, 552-563
26. Birsoy, K., Wang, T., Chen, W. W., Freinkman, E., Abu-Remaileh, M., and Sabatini, D. M. (2015) An essential role of the mitochondrial electron transport chain in cell proliferation is to enable aspartate synthesis. Cell 162, 540-551