Alterations in cellular metabolome after pharmacological inhibition of Notch in glioblastoma cells

International Journal of Cancer

Volumn 138, Issue 5, 2016, Pages 1246-1255

  Kahlert, Ulf D ^a,b   Cheng, Menglin ^a   Koch, Katharina ^b   Marchionni, Luigi ^a,c   Fan, Xing ^d   Raabe, Eric H ^a,c   Maciaczyk, Jarek ^b   Glunde, Kristine ^a,c   Eberhart, Charles G ^a  

^a JOHNS HOPKINS HOSPITAL   (United States)

^b University Medical Center   (Germany)

^c JOHNS HOPKINS UNIVERSITY   (United States)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

GBM; glioma; glutamate; glutaminase; glycolysis; GSI; metabolism; MRK003; Notch; WNT

Indexed keywords

GLUTAMIC ACID; GLUTAMINASE; LGK 974; MAMMALIAN TARGET OF RAPAMYCIN; MRK 003; NOTCH RECEPTOR; PROTEIN INHIBITOR; SAPANISERTIB; TEMOZOLOMIDE; UNCLASSIFIED DRUG; WNT PROTEIN; SULFOXIDE; THIADIAZOLE DERIVATIVE;

APOPTOSIS; ARTICLE; CANCER INHIBITION; CELL GROWTH; COLORIMETRY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME REPRESSION; FETUS; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE TARGETING; GENETIC TRANSCRIPTION; GLIOBLASTOMA CELL LINE; HUMAN; HUMAN CELL; METABOLOMICS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN HOMEOSTASIS; PROTON NUCLEAR MAGNETIC RESONANCE; WESTERN BLOTTING; ANTAGONISTS AND INHIBITORS; BRAIN NEOPLASMS; GLIOBLASTOMA; HOMEOSTASIS; METABOLISM; METABOLOME; TUMOR CELL LINE;

BRAIN NEOPLASMS; CELL LINE, TUMOR; CYCLIC S-OXIDES; GLIOBLASTOMA; GLUTAMIC ACID; GLUTAMINASE; HOMEOSTASIS; HUMANS; METABOLOME; RECEPTORS, NOTCH; THIADIAZOLES;

EID: 84955473956     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.29873     Document Type: Article

References (48)

1. Stupp R, Mason WP, van den Bent MJ, et al., Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 2005; 352: 987-96.
2. Lathia JD, Mack SC, Mulkearns-Hubert EE, et al., Cancer stem cells in glioblastoma. Genes Dev 2015; 29: 1203-17.
3. Takebe N, Miele L, Harris PJ, et al., Targeting Notch, Hedgehog, and Wnt pathways in cancer stem cells: clinical update. Nat Rev Clin Oncol 2015; 12: 445-64.
4. Harper JA, Yuan JS, Tan JB, et al., Notch signaling in development and disease. Clin Genet 2003; 64: 461-72.
5. Aguirre A, Rubio ME, Gallo V., Notch and EGFR pathway interaction regulates neural stem cell number and self-renewal. Nature 2010; 467: 323-7.
6. Allenspach EJ, Maillard I, Aster JC, et al., Notch signaling in cancer. Cancer Biol Ther 2002; 1: 466-76.
7. Teodorczyk M, Schmidt MHH., Notching on cancer's door: Notch signaling in brain tumors. Front Oncol 2014; 4: 341.
8. Dang CV., Links between metabolism and cancer. Genes Dev 2012; 26: 877-90.
9. Bi P, Shan T, Liu W, et al., Inhibition of Notch signaling promotes browning of white adipose tissue and ameliorates obesity. Nat Med 2014; 20: 911-18.
10. Ciofani M, Zúñiga-Pflücker JC., Notch promotes survival of pre-T cells at the beta-selection checkpoint by regulating cellular metabolism. Nat Immunol 2005; 6: 881-8.
11. Maekawa Y, Ishifune C, Tsukumo S-I, et al., Notch controls the survival of memory CD4+ T cells by regulating glucose uptake. Nat Med 2015; 21: 55-61.
12. Basak NP, Roy A, Banerjee S., Alteration of mitochondrial proteome due to activation of Notch1 signaling pathway. J Biol Chem 2014; 289: 7320-34.
13. Landor SK-J, Mutvei AP, Mamaeva V, et al., Hypo- and hyperactivated Notch signaling induce a glycolytic switch through distinct mechanisms. Proc Natl Acad Sci USA 2011; 108: 18814-19.
14. Fan X, Khaki L, Zhu TS, et al., NOTCH pathway blockade depletes CD133-positive glioblastoma cells and inhibits growth of tumor neurospheres and xenografts. Stem Cells Dayt Ohio 2010; 28: 5-16.
15. de Groot J, Sontheimer H., Glutamate and the biology of gliomas. Glia 2011; 59: 1181-9.
16. Kahlert UD, Bender NO, Maciaczyk D, et al., CD133/CD15 defines distinct cell subpopulations with differential in vitro clonogenic activity and stem cell-related gene expression profile in in vitro propagated glioblastoma multiforme-derived cell line with a PNET-like component. Folia Neuropathol Assoc Pol Neuropathol Med Res Cent Pol Acad Sci 2012; 50: 357-68.
17. Heaphy CM, Schreck KC, Raabe E, et al., A glioblastoma neurosphere line with alternative lengthening of telomeres. Acta Neuropathol (Berl) 2013; 126: 607-8.
18. Lopez WOC, Nikkhah G, Kahlert UD, et al., Clinical neurotransplantation protocol for Huntington's and Parkinson's disease. Restor Neurol Neurosci 2013; 31: 579-95.
19. Glunde K, Shah T, Winnard PT, et al., Hypoxia regulates choline kinase expression through hypoxia-inducible factor-1 alpha signaling in a human prostate cancer model. Cancer Res 2008; 68: 172-80.
20. Schreck KC, Taylor P, Marchionni L, et al., The Notch target Hes1 directly modulates Gli1 expression and Hedgehog signaling: a potential mechanism of therapeutic resistance. Clin Cancer Res 2010; 16: 6060-70.
21. Kortenhorst MSQ, Wissing MD, Rodríguez R, et al., Analysis of the genomic response of human prostate cancer cells to histone deacetylase inhibitors. Epigenetics 2013; 8: 907-20.
22. García-García C, Ibrahim YH, Serra V, et al., Dual mTORC1/2 and HER2 blockade results in antitumor activity in preclinical models of breast cancer resistant to anti-HER2 therapy. Clin Cancer Res 2012; 18: 2603-12.
23. Liu J, Pan S, Hsieh MH, et al., Targeting Wnt-driven cancer through the inhibition of Porcupine by LGK974. Proc Natl Acad Sci USA 2013; 110: 20224-9.
24. Wang J-B, Erickson JW, Fuji R, et al., Targeting mitochondrial glutaminase activity inhibits oncogenic transformation. Cancer Cell 2010; 18: 207-19.
25. Fuerer C, Nusse R., Lentiviral vectors to probe and manipulate the Wnt signaling pathway. PLoS One 2010; 5: e9370.
26. Kahlert UD, Suwala AK, Koch K, et al., Pharmacologic Wnt inhibition reduces proliferation, survival, and clonogenicity of glioblastoma cells. J Neuropathol Exp Neurol 2015; 74: 889-900.
27. Saito N, Fu J, Zheng S, et al., A high Notch pathway activation predicts response to γ secretase inhibitors in proneural subtype of glioma tumor-initiating cells. Stem Cells 2014; 32: 301-12.
28. Zhang K, Zhang J, Han L, et al., Wnt/beta-catenin signaling in glioma. J Neuroimmune Pharmacol 2012; 7: 740-9.
29. Bolõs V, Grego-Bessa J, de la Pompa JL., Notch signaling in development and cancer. Endocr Rev 2007; 28: 339-63.
30. Gillies RJ, Barry JA, Ross BD., In vitro and in vivo 13C and 31P NMR analyses of phosphocholine metabolism in rat glioma cells. Magn Reson Med 1994; 32: 310-18.
31. Dali-Youcef N, Froelich S, Moussallieh F-M, et al., Gene expression mapping of histone deacetylases and co-factors, and correlation with survival time and 1H-HRMAS metabolomic profile in human gliomas. Sci Rep 2015; 5: 9087.
32. Righi V, Andronesi OC, Mintzopoulos D, et al., High-resolution magic angle spinning magnetic resonance spectroscopy detects glycine as a biomarker in brain tumors. Int J Oncol 2010; 36: 301-6.
33. Al-Saffar NMS, Marshall LV, Jackson LE, et al., Lactate and choline metabolites detected in vitro by nuclear magnetic resonance spectroscopy are potential metabolic biomarkers for PI3K inhibition in pediatric glioblastoma. PLoS One 2014; 9: e103835.
34. Venkatesh HS, Chaumeil MM, Ward CS, et al., Reduced phosphocholine and hyperpolarized lactate provide magnetic resonance biomarkers of PI3K/Akt/mTOR inhibition in glioblastoma. Neuro Oncol 2012; 14: 315-25.
35. Kim D, Fiske BP, Birsoy K, et al., SHMT2 drives glioma cell survival in ischaemia but imposes a dependence on glycine clearance. Nature 2015; 520: 363-7.
36. Bar EE, Lin A, Mahairaki V, et al., Hypoxia increases the expression of stem-cell markers and promotes clonogenicity in glioblastoma neurospheres. Am J Pathol 2010; 177: 1491-502.
37. Jain M, Nilsson R, Sharma S, et al., Metabolite profiling identifies a key role for glycine in rapid cancer cell proliferation. Science 2012; 336: 1040-4.
38. Xu J, Chi F, Guo T, et al., NOTCH reprograms mitochondrial metabolism for proinflammatory macrophage activation. J Clin Invest 2015; 125: 1579-90.
39. Guidoni L, Ricci-Vitiani L, Rosi A, et al., (1)H NMR detects different metabolic profiles in glioblastoma stem-like cells. NMR Biomed 2014; 27: 129-45.
40. Ramm P, Bettscheider M, Beier D, et al., 1H-nuclear magnetic resonance spectroscopy of glioblastoma cancer stem cells. Stem Cells Dev 2011; 20: 2189-95.
41. Angulo-Rojo C, Manning-Cela R, Aguirre A, et al., Involvement of the Notch pathway in terminal astrocytic differentiation: role of PKA. ASN Neuro 2013; 5: e00130.
42. Chen R, Nishimura MC, Kharbanda S, et al., Hominoid-specific enzyme GLUD2 promotes growth of IDH1R132H glioma. Proc Natl Acad Sci USA 2014; 111: 14217-22.
43. Cuperlovic-Culf M, Ferguson D, Culf A, et al., 1H NMR metabolomics analysis of glioblastoma subtypes: correlation between metabolomics and gene expression characteristics. J Biol Chem 2012; 287: 20164-75.
44. Cassago A, Ferreira APS, Ferreira IM, et al., Mitochondrial localization and structure-based phosphate activation mechanism of Glutaminase C with implications for cancer metabolism. Proc Natl Acad Sci USA 2012; 109: 1092-7.
45. Gao P, Tchernyshyov I, Chang T-C, et al., cMyc suppression of miR-23a/b enhances mitochondrial glutaminase expression and glutamine metabolism. Nature 2009; 458: 762-5.
46. Seltzer MJ, Bennett BD, Joshi AD, et al., Inhibition of glutaminase preferentially slows growth of glioma cells with mutant IDH1. Cancer Res 2010; 70: 8981-7.
47. Stalnecker CA, Ulrich SM, Li Y, et al., Mechanism by which a recently discovered allosteric inhibitor blocks glutamine metabolism in transformed cells. Proc Natl Acad Sci USA 2015; 112: 394-9.
48. Tanaka K, Sasayama T, Irino Y, et al., Compensatory glutamine metabolism promotes glioblastoma resistance to mTOR inhibitor treatment. J Clin Invest 2015; 125: 1591-602.