Clinical aggressiveness of malignant gliomas is linked to augmented metabolism of amino acids

Journal of Neuro-Oncology

Volumn 128, Issue 1, 2016, Pages 57-66

  Panosyan, Eduard H ^a   Lasky, Joseph L ^a   Lin, Henry J ^a   Lai, Albert ^b   Hai, Yang ^a   Guo, Xiuqing ^a   Quinn, Michael ^c   Nelson, Stanley F ^d   Cloughesy, Timothy F ^b   Nghiemphu, P Leia ^b  

^a LOS ANGELES BIOMEDICAL RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c SiliconMED North America Inc   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Asparagine; Branched chain amino acids; Glioma; Glutamine; Metabolism

Indexed keywords

ASPARAGINE; ASPARTATE AMMONIA LIGASE; BRANCHED CHAIN AMINO ACID; BRANCHED CHAIN AMINO ACID AMINOTRANSFERASE; BRANCHED CHAIN AMINO ACID AMINOTRANSFERASE 1; GLUTAMINASE; GLUTAMINE; ISOCITRATE DEHYDROGENASE 1; TEMOZOLOMIDE; UNCLASSIFIED DRUG; AMINO ACID;

ADJUVANT CHEMOTHERAPY; ADULT; AMINO ACID METABOLISM; ANAPLASTIC MIXED GLIOMA; ARTICLE; CANCER GRADING; CANCER RADIOTHERAPY; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GLIOBLASTOMA; GLIOMA; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; OLIGODENDROGLIOMA; OVERALL SURVIVAL; PROGRESSION FREE SURVIVAL; TUMOR GROWTH; TUMOR RECURRENCE; BRAIN TUMOR; GENE EXPRESSION REGULATION; GENETICS; KAPLAN MEIER METHOD; METABOLISM; MIDDLE AGED; MULTIVARIATE ANALYSIS; PATHOPHYSIOLOGY; TREATMENT OUTCOME; TUMOR INVASION;

AMINO ACIDS; BRAIN NEOPLASMS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOMA; HUMANS; KAPLAN-MEIER ESTIMATE; MALE; MIDDLE AGED; MULTIVARIATE ANALYSIS; NEOPLASM INVASIVENESS; NEOPLASM RECURRENCE, LOCAL; TREATMENT OUTCOME;

EID: 84971317380     PISSN: 0167594X     EISSN: 15737373     Source Type: Journal    
DOI: 10.1007/s11060-016-2073-5     Document Type: Article

References (34)

1. Wolf A, Agnihotri S, Guha A (2010) Targeting metabolic remodeling in glioblastoma multiforme. Oncotarget 1(7):567
2. la Fougère C, Suchorska B, Bartenstein P, Kreth F-W, Tonn J-C (2011) Molecular imaging of gliomas with PET: opportunities and limitations. Neuro-Oncology 13:806–819. doi:10.1093/neuonc/nor054
3. Langen K-J, Tatsch K, Grosu A-L, Jacobs AH, Weckesser M, Sabri O (2008) Diagnostics of cerebral gliomas with radiolabeled amino acids. Dtsch Arztebl Int 105:55–61. doi:10.3238/arztebl.2008.0055
4. Galldiks N, Langen K (2014) Applications of PET imaging of neurological tumors with radiolabeled amino acids. Q J Nucl Med Mol Imaging 59(1):70–82
5. Dranoff G, Elion GB, Friedman HS, Bigner DD (1985) Combination chemotherapy in vitro exploiting glutamine metabolism of human glioma and medulloblastoma. Cancer Res 45:4082–4086
6. Panosyan EH, Wang Y, Xia P, Lee W-NP, Pak Y, Laks DR, Lin HJ, Moore TB, Cloughesy TF, Kornblum HI, Lasky JL (2014) Asparagine depletion potentiates the cytotoxic effect of chemotherapy against brain tumors. Mol Cancer Res 12:694–702. doi:10.1158/1541-7786.mcr-13-0576
7. Seltzer MJ, Bennett BD, Joshi AD, Gao P, Thomas AG, Ferraris DV, Tsukamoto T, Rojas CJ, Slusher BS, Rabinowitz JD, Dang CV, Riggins GJ (2010) Inhibition of glutaminase preferentially slows growth of glioma cells with mutant IDH1. Cancer Res 70:8981–8987. doi:10.1158/0008-5472.can-10-1666
8. Taylor SA, Crowley J, Pollock TW, Eyre HJ, Jaeckle C, Hynes HE, Stephens RL (1991) Objective antitumor activity of acivicin in patients with recurrent CNS malignancies: a Southwest Oncology Group trial. J Clin Oncol 9:1476–1479
9. Chang SM, Kuhn JG, Robins HI, Schold SC, Spence AM, Berger MS, Mehta MP, Bozik ME, Pollack I, Schiff D, Gilbert M, Rankin C, Prados MD (1999) Phase II study of phenylacetate in patients with recurrent malignant glioma: a North American brain tumor consortium report. J Clin Oncol 17:984
10. Tonjes M, Barbus S, Park YJ, Wang W, Schlotter M, Lindroth AM, Pleier SV, Bai AHC, Karra D, Piro RM, Felsberg J, Addington A, Lemke D, Weibrecht I, Hovestadt V, Rolli CG, Campos B, Turcan S, Sturm D, Witt H, Chan TA, Herold-Mende C, Kemkemer R, Konig R, Schmidt K, Hull W-E, Pfister SM, Jugold M, Hutson SM, Plass C, Okun JG, Reifenberger G, Lichter P, Radlwimmer B (2013) BCAT1 promotes cell proliferation through amino acid catabolism in gliomas carrying wild-type IDH1. Nat Med 19:901–908. doi:10.1038/nm.3217.html#supplementary-information.
11. Balasubramanian MN, Butterworth EA, Kilberg MS (2013) Asparagine synthetase: regulation by cell stress and involvement in tumor biology 304(8):E789–E799
12. Wise DR, Thompson CB (2010) Glutamine addiction: a new therapeutic target in cancer. Trends Biochem Sci 35:427–433. doi:10.1016/j.tibs.2010.05.003
13. Agnihotri S, Aldape KD, Zadeh G (2014) Isocitrate dehydrogenase status and molecular subclasses of glioma and glioblastoma. Neurosurg Focus 37:E13. doi:10.3171/2014.9.focus14505
14. Reitman ZJ, Jin G, Karoly ED, Spasojevic I, Yang J, Kinzler KW, He Y, Bigner DD, Vogelstein B, Yan H (2011) Profiling the effects of isocitrate dehydrogenase 1 and 2 mutations on the cellular metabolome. Proc Natl Acad Sci 108:3270–3275. doi:10.1073/pnas.1019393108
15. Venneti S, Thompson CB (2013) Metabolic modulation of epigenetics in gliomas. Brain Pathol 23:217–221. doi:10.1111/bpa.12022
16. Bender DA (2012) Amino acids synthesized from glutamate: glutamine, proline, ornithine, citrulline and arginine. Amino acid metabolism. Wiley, New York, pp 157–223
17. Zhang J, Fan J, Venneti S, Cross Justin R, Takagi T, Bhinder B, Djaballah H, Kanai M, Cheng Emily H, Judkins Alexander R, Pawel B, Baggs J, Cherry S, Rabinowitz Joshua D, Thompson Craig B (2014) Asparagine plays a critical role in regulating cellular adaptation to glutamine depletion. Mol Cell 56:205–218. doi:10.1016/j.molcel.2014.08.018
18. Lee Y, Scheck A, Cloughesy T, Lai A, Dong J, Farooqi H, Liau L, Horvath S, Mischel P, Nelson S (2008) Gene expression analysis of glioblastomas identifies the major molecular basis for the prognostic benefit of younger age. BMC Med Genom 1:52
19. http://probesetanalyzer.com/
20. Mareninov S, De Jesus J, Sanchez D, Kay A, Wilson R, Babic I, Chen W, Telesca D, Lou J, Mirsadraei L, Gardner T, Khanlou N, Vinters H, Shafa B, Lai A, Liau L, Mischel P, Cloughesy T, Yong W (2013) Lyophilized brain tumor specimens can be used for histologic, nucleic acid, and protein analyses after 1 year of room temperature storage. J Neurooncol 113:365–373. doi:10.1007/s11060-013-1135-1
21. Chou AP, Chowdhury R, Li S, Chen W, Kim AJ, Piccioni DE, Selfridge JM, Mody RR, Chang S, Lalezari S, Lin J, Sanchez DE, Wilson RW, Garrett MC, Harry B, Mottahedeh J, Nghiemphu PL, Kornblum HI, Mischel PS, Prins RM, Yong WH, Cloughesy T, Nelson SF, Liau LM, Lai A (2012) Identification of retinol binding protein 1 promoter hypermethylation in isocitrate dehydrogenase 1 and 2 mutant gliomas. J Natl Cancer Inst 104:1458–1469. doi:10.1093/jnci/djs357
22. Weller M, Cloughesy T, Perry JR, Wick W (2013) Standards of care for treatment of recurrent glioblastoma—are we there yet? Neuro-Oncology 15:4–27. doi:10.1093/neuonc/nos273
23. Squatrito M, Holland EC (2011) DNA damage response and growth factor signaling pathways in gliomagenesis and therapeutic resistance. Cancer Res 71:5945–5949. doi:10.1158/0008-5472.can-11-1245
24. Khasraw M, Ameratunga MS, Grant R, Wheeler H, Pavlakis N (2014) Antiangiogenic therapy for high-grade glioma. Cochrane Database Syst Rev 9:CD008218. doi:10.1002/14651858.CD008218.pub3
25. Patel M, Kim J, Ruzevick J, Li G, Lim M (2014) The future of glioblastoma therapy: synergism of standard of care and immunotherapy. Cancers 6:1953–1985
26. Marie SKN, Shinjo SMO (2011) Metabolism and brain cancer. Clinics 66:33–43
27. Weinberg SE, Chandel NS (2015) Targeting mitochondria metabolism for cancer therapy. Nat Chem Biol 11:9–15. doi:10.1038/nchembio.1712
28. Avramis VI, Panosyan EH (2005) Pharmacokinetic/pharmacodynamic relationships of asparaginase formulations: the past, the present and recommendations for the future. Clin Pharmacokinet 44:367–393
29. Stathias V, Pastori C, Griffin TZ, Komotar R, Clarke J, Zhang M, Ayad NG (2014) Identifying glioblastoma gene networks based on hypergeometric test analysis. PLoS ONE 9:e115842. doi:10.1371/journal.pone.0115842
30. Hart MG, Garside R, Rogers G, Stein K, Grant R (2013) Temozolomide for high grade glioma. Cochrane Database Syst Rev 4:CD007415. doi:10.1002/14651858.CD007415.pub2
31. Wu S-H, Bi J-F, Cloughesy T, Cavenee WK, Mischel PS (2014) Emerging function of mTORC2 as a core regulator in glioblastoma: metabolic reprogramming and drug resistance. Cancer Biol Med 11:255–263. doi:10.7497/j.issn.2095-3941.2014.04.004
32. Gao Q, Lei T, Ye F (2013) Therapeutic targeting of EGFR-activated metabolic pathways in glioblastoma. Expert Opin Investig Drugs 22:1023–1040. doi:10.1517/13543784.2013.806484
33. . http://hgserver1.amc.nl/cgi-bin/r2/main.cgi
34. Gross MI, Demo SD, Dennison JB, Chen L, Chernov-Rogan T, Goyal B, Janes JR, Laidig GJ, Lewis ER, Li J, MacKinnon AL, Parlati F, Rodriguez MLM, Shwonek PJ, Sjogren EB, Stanton TF, Wang T, Yang J, Zhao F, Bennett MK (2014) Antitumor activity of the glutaminase inhibitor CB-839 in triple-negative breast cancer. Mol Cancer Ther 13:890–901. doi:10.1158/1535-7163.mct-13-0870