PHGDH Defines a Metabolic Subtype in Lung Adenocarcinomas with Poor Prognosis

Cell Reports

Volumn 19, Issue 11, 2017, Pages 2289-2303

  Zhang, Boxi ^a   Zheng, Adi ^a   Hydbring, Per ^a   Ambroise, Gorbatchev ^a   Ouchida, Amanda Tomie ^a   Goiny, Michel ^a   Vakifahmetoglu Norberg, Helin ^a   Norberg, Erik ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

DNA damage; lung adenocarcinoma; lung cancer; metabolic heterogeneity; metabolomics; PHGDH; purines; pyrimidines; serine; tumor metabolism

Indexed keywords

CARBON; DEUBIQUITINASE; GLUTATHIONE; JOSEPHIN DOMAIN CONTAINING 2; PHOSPHOGLYCERATE DEHYDROGENASE; PURINE; PYRIMIDINE; SERINE; UNCLASSIFIED DRUG; DNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOSYNTHESIS; CANCER PROGNOSIS; CARCINOGENICITY; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; ENZYME DEGRADATION; FEMALE; HUMAN; HUMAN CELL; LUNG ADENOCARCINOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN STABILITY; UBIQUITINATION; ADENOCARCINOMA; ANIMAL; ENZYMOLOGY; GENETICS; LUNG TUMOR; METABOLISM; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; PROGNOSIS; SCID MOUSE; TUMOR CELL LINE; XENOGRAFT;

ADENOCARCINOMA; ANIMALS; CELL LINE, TUMOR; CELL PROLIFERATION; DNA, NEOPLASM; FEMALE; HETEROGRAFTS; HUMANS; LUNG NEOPLASMS; MICE; MICE, NUDE; MICE, SCID; PHOSPHOGLYCERATE DEHYDROGENASE; PROGNOSIS; SERINE;

EID: 85020712800     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2017.05.067     Document Type: Article

References (44)

1. Baek, G., Tse, Y.F., Hu, Z., Cox, D., Buboltz, N., McCue, P., Yeo, C.J., White, M.A., DeBerardinis, R.J., Knudsen, E.S., Witkiewicz, A.K., MCT4 defines a glycolytic subtype of pancreatic cancer with poor prognosis and unique metabolic dependencies. Cell Rep. 9 (2014), 2233–2249.
2. Bolstad, B.M., Irizarry, R.A., Astrand, M., Speed, T.P., A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19 (2003), 185–193.
3. Boroughs, L.K., DeBerardinis, R.J., Metabolic pathways promoting cancer cell survival and growth. Nat. Cell Biol. 17 (2015), 351–359.
4. Botling, J., Edlund, K., Lohr, M., Hellwig, B., Holmberg, L., Lambe, M., Berglund, A., Ekman, S., Bergqvist, M., Ponten, F., et al. Biomarker discovery in non-small cell lung cancer: integrating gene expression profiling, meta-analysis, and tissue microarray validation. Clin Cancer Res. 19 (2013), 194–204.
5. Buescher, J.M., Antoniewicz, M.R., Boros, L.G., Burgess, S.C., Brunengraber, H., Clish, C.B., DeBerardinis, R.J., Feron, O., Frezza, C., Ghesquiere, B., et al. A roadmap for interpreting (13)C metabolite labeling patterns from cells. Curr. Opin. Biotechnol. 34 (2015), 189–201.
6. Cantor, J.R., Sabatini, D.M., Cancer cell metabolism: one hallmark, many faces. Cancer Discov. 2 (2012), 881–898.
7. Caro, P., Kishan, A.U., Norberg, E., Stanley, I.A., Chapuy, B., Ficarro, S.B., Polak, K., Tondera, D., Gounarides, J., Yin, H., et al. Metabolic signatures uncover distinct targets in molecular subsets of diffuse large B cell lymphoma. Cancer Cell 22 (2012), 547–560.
8. Chokkathukalam, A., Jankevics, A., Creek, D.J., Achcar, F., Barrett, M.P., Breitling, R., mzMatch-ISO: an R tool for the annotation and relative quantification of isotope-labelled mass spectrometry data. Bioinformatics 29 (2013), 281–283.
9. DeNicola, G.M., Chen, P.H., Mullarky, E., Sudderth, J.A., Hu, Z., Wu, D., Tang, H., Xie, Y., Asara, J.M., Huffman, K.E., et al. NRF2 regulates serine biosynthesis in non-small cell lung cancer. Nat. Genet. 47 (2015), 1475–1481.
10. Gentleman, R.C., Carey, V.J., Bates, D.M., Bolstad, B., Dettling, M., Dudoit, S., Ellis, B., Gautier, L., Ge, Y., Gentry, J., et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol., 5, 2004, R80.
11. Gerdes, M.J., Sood, A., Sevinsky, C., Pris, A.D., Zavodszky, M.I., Ginty, F., Emerging understanding of multiscale tumor heterogeneity. Front. Oncol., 4, 2014, 366.
12. Gerlinger, M., Rowan, A.J., Horswell, S., Larkin, J., Endesfelder, D., Gronroos, E., Martinez, P., Matthews, N., Stewart, A., Tarpey, P., et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med. 366 (2012), 883–892.
13. Hao, H.X., Khalimonchuk, O., Schraders, M., Dephoure, N., Bayley, J.P., Kunst, H., Devilee, P., Cremers, C.W., Schiffman, J.D., Bentz, B.G., et al. SDH5, a gene required for flavination of succinate dehydrogenase, is mutated in paraganglioma. Science 325 (2009), 1139–1142.
14. Hensley, C.T., Faubert, B., Yuan, Q., Lev-Cohain, N., Jin, E., Kim, J., Jiang, L., Ko, B., Skelton, R., Loudat, L., et al. Metabolic Heterogeneity in Human Lung Tumors. Cell 164 (2016), 681–694.
15. Kampf, C., Olsson, I., Ryberg, U., Sjӧstedt, E., Pontén, F., Production of tissue microarrays, immunohistochemistry staining and digitalization within the human protein atlas. J Vis Exp., 63, 2012, 3620.
16. Kim, H.S., Mendiratta, S., Kim, J., Pecot, C.V., Larsen, J.E., Zubovych, I., Seo, B.Y., Kim, J., Eskiocak, B., Chung, H., et al. Systematic identification of molecular subtype-selective vulnerabilities in non-small-cell lung cancer. Cell 155 (2013), 552–566.
17. Lane, A.N., Fan, T.W., Regulation of mammalian nucleotide metabolism and biosynthesis. Nucleic Acids Res. 43 (2015), 2466–2485.
18. Locasale, J.W., Serine, glycine and one-carbon units: cancer metabolism in full circle. Nat. Rev. Cancer 13 (2013), 572–583.
19. Locasale, J.W., Grassian, A.R., Melman, T., Lyssiotis, C.A., Mattaini, K.R., Bass, A.J., Heffron, G., Metallo, C.M., Muranen, T., Sharfi, H., et al. Phosphoglycerate dehydrogenase diverts glycolytic flux and contributes to oncogenesis. Nat. Genet. 43 (2011), 869–874.
20. Lord, C.J., Ashworth, A., The DNA damage response and cancer therapy. Nature 481 (2012), 287–294.
21. Maddocks, O.D., Berkers, C.R., Mason, S.M., Zheng, L., Blyth, K., Gottlieb, E., Vousden, K.H., Serine starvation induces stress and p53-dependent metabolic remodelling in cancer cells. Nature 493 (2013), 542–546.
22. Mardis, E.R., Ding, L., Dooling, D.J., Larson, D.E., Mclellan, M.D., Chen, K., Koboldt, D.C., Fulton, R., Delehaunty, K.D., Mcgrath, S.D., et al. Recurring mutations found by sequencing an acute myeloid leukemia genome. N Engl J Med. 361 (2009), 1058–1066.
23. Mattaini, K.R., Sullivan, M.R., Vander Heiden, M.G., The importance of serine metabolism in cancer. J. Cell Biol. 214 (2016), 249–257.
24. Nijman, S.M., Luna-Vargas, M.P., Velds, A., Brummelkamp, T.R., Dirac, A.M., Sixma, T.K., Bernards, R., A genomic and functional inventory of deubiquitinating enzymes. Cell 123 (2005), 773–786.
25. Norberg, E., Karlsson, M., Korenovska, O., Szydlowski, S., Silberberg, G., Uhlen, P., Orrenius, S., Zhivotovsky, B., Critical role for hyperpolarization-activated cyclic nucleotide-gated channel 2 in the AIF-mediated apoptosis. EMBO J. 29 (2010), 3869–3878.
26. Okayama, H., Kohno, T., Ishii, Y., Shimada, Y., Shiraishi, K., Iwakawa, R., Furuta, K., Tsuta, K., Shibata, T., Yamamoto, S., et al. Identification of genes upregulated in ALK-positive and EGFR/KRAS/ALK-negative lung adenocarcinomas. Cancer Res. 72 (2012), 100–111.
27. Pollard, P.J., Wortham, N.C., Tomlinson, I.P., The TCA cycle and tumorigenesis: the examples of fumarate hydratase and succinate dehydrogenase. Ann. Med. 35 (2003), 632–639.
28. Possemato, R., Marks, K.M., Shaul, Y.D., Pacold, M.E., Kim, D., Birsoy, K., Sethumadhavan, S., Woo, H.K., Jang, H.G., Jha, A.K., et al. Functional genomics reveal that the serine synthesis pathway is essential in breast cancer. Nature 476 (2011), 346–350.
29. Postel-Vinay, S., Vanhecke, E., Olaussen, K.A., Lord, C.J., Ashworth, A., Soria, J.C., The potential of exploiting DNA-repair defects for optimizing lung cancer treatment. Nat. Rev. Clin. Oncol. 9 (2012), 144–155.
30. Sancar, A., Lindsey-Boltz, L.A., Unsal-Kaçmaz, K., Linn, S., Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 73 (2004), 39–85.
31. Scheltema, R.A., Jankevics, A., Jansen, R.C., Swertz, M.A., Breitling, R., PeakML/mzMatch: a file format, Java library, R library, and tool-chain for mass spectrometry data analysis. Anal Chem. 83 (2011), 2786–2793.
32. Sellers, K., Fox, M.P., Bousamra, M. 2nd, Slone, S.P., Higashi, R.M., Miller, D.M., Wang, Y., Yan, J., Yuneva, M.O., Deshpande, R., et al. Pyruvate carboxylase is critical for non-small-cell lung cancer proliferation. J. Clin. Invest. 125 (2015), 687–698.
33. Snell, K., Enzymes of serine metabolism in normal, developing and neoplastic rat tissues. Adv Enzyme Regul. 22 (1984), 325–400.
34. Snell, K., Fell, D.A., Metabolic control analysis of mammalian serine metabolism. Adv Enzyme Regul. 30 (1990), 13–32.
35. Sowa, M.E., Bennett, E.J., Gygi, S.P., Harper, J.W., Defining the human deubiquitinating enzyme interaction landscape. Cell 138 (2009), 389–403.
36. Stanley, I.A., Ribeiro, S.M., Giménez-Cassina, A., Norberg, E., Danial, N.N., Changing appetites: the adaptive advantages of fuel choice. Trends Cell Biol. 24 (2014), 118–127.
37. Subramanian, A., Tamayo, P., Mootha, V.K., Mukherjee, S., Ebert, B.L., Gillette, M.A., Paulovich, A., Pomeroy, S.L., Golub, T.R., Lander, E.S., Mesirov, J.P., Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 102 (2005), 15545–15550.
38. Tautenhahn, R., Bӧttcher, C., Neumann, S., Highly sensitive feature detection for high resolution LC/MS. BMC Bioinformatics, 28, 2008, 504.
39. Thompson, C.B., Metabolic enzymes as oncogenes or tumor suppressors. N. Engl. J. Med. 360 (2009), 813–815.
40. Travis, W.D., Brambilla, E., Riely, G.J., New pathologic classification of lung cancer: relevance for clinical practice and clinical trials. J. Clin. Oncol. 31 (2013), 992–1001.
41. Vakifahmetoglu-Norberg, H., Ouchida, A.T., Norberg, E., The role of mitochondria in metabolism and cell death. Biochem. Biophys. Res. Commun. 482 (2017), 426–431.
42. Vander Heiden, M.G., Targeting cancer metabolism: a therapeutic window opens. Nat. Rev. Drug Discov. 10 (2011), 671–684.
43. Yang, M., Vousden, K.H., Serine and one-carbon metabolism in cancer. Nat. Rev. Cancer 16 (2016), 650–662.
44. Yu, G., He, Q.Y., ReactomePA: an R/Bioconductor package for reactome pathway analysis and visualization. Mol Biosyst. 12 (2016), 477–479.