The contribution of ketone bodies to glycolytic inhibition for the treatment of adult and pediatric glioblastoma (original) (raw)

References

1. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, Ludwin SK, Gorlia T, Allgeier A, Lacombe D, Cairncross JG, Eisenhauer E, Mirimanoff RO, European Organisation for R, Treatment of Cancer Brain T, Radiotherapy G, National Cancer Institute of Canada Clinical Trials G (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352(10):987–996. https://doi.org/10.1056/NEJMoa043330
   Article CAS PubMed Google Scholar
2. Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC, Ludwin SK, Allgeier A, Fisher B, Belanger K, Hau P, Brandes AA, Gijtenbeek J, Marosi C, Vecht CJ, Mokhtari K, Wesseling P, Villa S, Eisenhauer E, Gorlia T, Weller M, Lacombe D, Cairncross JG, Mirimanoff RO, European Organisation for R, Treatment of Cancer Brain T, Radiation Oncology G, National Cancer Institute of Canada Clinical Trials G (2009) Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol 10(5):459–466. https://doi.org/10.1016/S1470-2045(09)70025-7
   Article CAS PubMed Google Scholar
3. Ostrom QT, Gittleman H, Liao P, Vecchione-Koval T, Wolinsky Y, Kruchko C, Barnholtz-Sloan JS (2017) CBTRUS statistical report: primary brain and other central nervous system tumors diagnosed in the United States in 2010–2014. Neuro Oncol 19:v1–v88. https://doi.org/10.1093/neuonc/nox158
   Article PubMed PubMed Central Google Scholar
4. Lathia JD, Mack SC, Mulkearns-Hubert EE, Valentim CL, Rich JN (2015) Cancer stem cells in glioblastoma. Genes Dev 29(12):1203–1217. https://doi.org/10.1101/gad.261982.115
   Article CAS PubMed PubMed Central Google Scholar
5. Chen J, Li Y, Yu TS, McKay RM, Burns DK, Kernie SG, Parada LF (2012) A restricted cell population propagates glioblastoma growth after chemotherapy. Nature 488(7412):522–526. https://doi.org/10.1038/nature11287
   Article CAS PubMed PubMed Central Google Scholar
6. Gimple RC, Bhargava S, Dixit D, Rich JN (2019) Glioblastoma stem cells: lessons from the tumor hierarchy in a lethal cancer. Genes Dev 33(11–12):591–609. https://doi.org/10.1101/gad.324301.119
   Article CAS PubMed PubMed Central Google Scholar
7. Duman C, Yaqubi K, Hoffmann A, Acikgoz AA, Korshunov A, Bendszus M, Herold-Mende C, Liu HK, Alfonso J (2019) Acyl-CoA-binding protein drives glioblastoma tumorigenesis by sustaining fatty acid oxidation. Cell Metab 30(2):274–289. https://doi.org/10.1016/j.cmet.2019.04.004
   Article CAS PubMed Google Scholar
8. Warburg O, Wind F, Negelein E (1927) The metabolism of tumors in the body. J Gen Physiol 8(6):519–530. https://doi.org/10.1085/jgp.8.6.519
   Article CAS PubMed PubMed Central Google Scholar
9. Albert NL, Weller M, Suchorska B, Galldiks N, Soffietti R, Kim MM, la Fougere C, Pope W, Law I, Arbizu J, Chamberlain MC, Vogelbaum M, Ellingson BM, Tonn JC (2016) Response Assessment in Neuro-Oncology working group and European Association for Neuro-Oncology recommendations for the clinical use of PET imaging in gliomas. Neuro Oncol 18(9):1199–1208. https://doi.org/10.1093/neuonc/now058
   Article CAS PubMed PubMed Central Google Scholar
10. Boutrid H, Jockovich ME, Murray TG, Pina Y, Feuer WJ, Lampidis TJ, Cebulla CM (2008) Targeting hypoxia, a novel treatment for advanced retinoblastoma. Invest Ophthalmol Vis Sci 49(7):2799–2805. https://doi.org/10.1167/iovs.08-1751
    Article PubMed Google Scholar
11. Maschek G, Savaraj N, Priebe W, Braunschweiger P, Hamilton K, Tidmarsh GF, De Young LR, Lampidis TJ (2004) 2-Deoxy-D-glucose increases the efficacy of adriamycin and paclitaxel in human osteosarcoma and non-small cell lung cancers in vivo. Cancer Res 64(1):31–34. https://doi.org/10.1158/0008-5472.can-03-3294
    Article CAS PubMed Google Scholar
12. Dwarakanath BS, Singh D, Banerji AK, Sarin R, Venkataramana NK, Jalali R, Vishwanath PN, Mohanti BK, Tripathi RP, Kalia VK, Jain V (2009) Clinical studies for improving radiotherapy with 2-deoxy-D-glucose: present status and future prospects. J Cancer Res Ther 5(Suppl 1):S21–26. https://doi.org/10.4103/0973-1482.55136
    Article CAS PubMed Google Scholar
13. Puchalska P, Crawford PA (2017) Multi-dimensional roles of ketone bodies in fuel metabolism, signaling, and therapeutics. Cell Metab 25(2):262–284. https://doi.org/10.1016/j.cmet.2016.12.022
    Article CAS PubMed PubMed Central Google Scholar
14. Shimazu T, Hirschey MD, Newman J, He W, Shirakawa K, Le Moan N, Grueter CA, Lim H, Saunders LR, Stevens RD, Newgard CB, Farese RV Jr, de Cabo R, Ulrich S, Akassoglou K, Verdin E (2013) Suppression of oxidative stress by beta-hydroxybutyrate, an endogenous histone deacetylase inhibitor. Science 339(6116):211–214. https://doi.org/10.1126/science.1227166
    Article CAS PubMed Google Scholar
15. Kanikarla-Marie P, Jain SK (2015) Hyperketonemia (acetoacetate) upregulates NADPH oxidase 4 and elevates oxidative stress, ICAM-1, and monocyte adhesivity in endothelial cells. Cell Physiol Biochem 35(1):364–373. https://doi.org/10.1159/000369702
    Article CAS PubMed PubMed Central Google Scholar
16. Nebeling LC, Miraldi F, Shurin SB, Lerner E (1995) Effects of a ketogenic diet on tumor metabolism and nutritional status in pediatric oncology patients: two case reports. J Am Coll Nutr 14(2):202–208. https://doi.org/10.1080/07315724.1995.10718495
    Article CAS PubMed Google Scholar
17. Schmidt M, Pfetzer N, Schwab M, Strauss I, Kammerer U (2011) Effects of a ketogenic diet on the quality of life in 16 patients with advanced cancer: a pilot trial. Nutr Metab (Lond) 8(1):54. https://doi.org/10.1186/1743-7075-8-54
    Article CAS Google Scholar
18. Zuccoli G, Marcello N, Pisanello A, Servadei F, Vaccaro S, Mukherjee P, Seyfried TN (2010) Metabolic management of glioblastoma multiforme using standard therapy together with a restricted ketogenic diet: case report. Nutr Metab (Lond) 7:33. https://doi.org/10.1186/1743-7075-7-33
    Article CAS Google Scholar
19. Gersey ZC, Rodriguez GA, Barbarite E, Sanchez A, Walters WM, Ohaeto KC, Komotar RJ, Graham RM (2017) Curcumin decreases malignant characteristics of glioblastoma stem cells via induction of reactive oxygen species. BMC Cancer 17(1):99. https://doi.org/10.1186/s12885-017-3058-2
    Article CAS PubMed PubMed Central Google Scholar
20. Sansalone L, Veliz EA, Myrthil NG, Stathias V, Walters W, Torrens II, Schurer SC, Vanni S, Leblanc RM, Graham RM (2019) Novel curcumin inspired bis-chalcone promotes endoplasmic reticulum stress and glioblastoma neurosphere cell death. Cancers (Basel). https://doi.org/10.3390/cancers11030357
    Article Google Scholar
21. Lee J, Kotliarova S, Kotliarov Y, Li A, Su Q, Donin NM, Pastorino S, Purow BW, Christopher N, Zhang W, Park JK, Fine HA (2006) Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell 9(5):391–403. https://doi.org/10.1016/j.ccr.2006.03.030
    Article CAS PubMed Google Scholar
22. Shah SS, Rodriguez GA, Musick A, Walters WM, de Cordoba N, Barbarite E, Marlow MM, Marples B, Prince JS, Komotar RJ, Vanni S, Graham RM (2019) Targeting glioblastoma stem cells with 2-deoxy-D-glucose (2-DG) potentiates radiation-induced unfolded protein response (UPR). Cancers (Basel). https://doi.org/10.3390/cancers11020159
    Article PubMed Google Scholar
23. Bowman RL, Wang Q, Carro A, Verhaak RG, Squatrito M (2017) GlioVis data portal for visualization and analysis of brain tumor expression datasets. Neuro Oncol 19(1):139–141. https://doi.org/10.1093/neuonc/now247
    Article CAS PubMed Google Scholar
24. Graham RM, Hernandez F, Puerta N, De Angulo G, Webster KA, Vanni S (2016) Resveratrol augments ER stress and the cytotoxic effects of glycolytic inhibition in neuroblastoma by downregulating Akt in a mechanism independent of SIRT1. Exp Mol Med 48:e210. https://doi.org/10.1038/emm.2015.116
    Article CAS PubMed PubMed Central Google Scholar
25. Chang HT, Olson LK, Schwartz KA (2013) Ketolytic and glycolytic enzymatic expression profiles in malignant gliomas: implication for ketogenic diet therapy. Nutr Metab (Lond) 10(1):47. https://doi.org/10.1186/1743-7075-10-47
    Article CAS Google Scholar
26. Nowicki MO, Dmitrieva N, Stein AM, Cutter JL, Godlewski J, Saeki Y, Nita M, Berens ME, Sander LM, Newton HB, Chiocca EA, Lawler S (2008) Lithium inhibits invasion of glioma cells; possible involvement of glycogen synthase kinase-3. Neuro Oncol 10(5):690–699. https://doi.org/10.1215/15228517-2008-041
    Article CAS PubMed PubMed Central Google Scholar
27. Chou CH, Chou AK, Lin CC, Chen WJ, Wei CC, Yang MC, Hsu CM, Lung FW, Loh JK, Howng SL, Hong YR (2012) GSK3beta regulates Bcl2L12 and Bcl2L12A anti-apoptosis signaling in glioblastoma and is inhibited by LiCl. Cell Cycle 11(3):532–542. https://doi.org/10.4161/cc.11.3.19051
    Article CAS PubMed Google Scholar
28. Korur S, Huber RM, Sivasankaran B, Petrich M, Morin P Jr, Hemmings BA, Merlo A, Lino MM (2009) GSK3beta regulates differentiation and growth arrest in glioblastoma. PLoS ONE 4(10):e7443. https://doi.org/10.1371/journal.pone.0007443
    Article CAS PubMed PubMed Central Google Scholar
29. Savage MW, Dhatariya KK, Kilvert A, Rayman G, Rees JA, Courtney CH, Hilton L, Dyer PH, Hamersley MS, Joint British Diabetes S (2011) Joint British Diabetes Societies guideline for the management of diabetic ketoacidosis. Diabet Med 28(5):508–515. https://doi.org/10.1111/j.1464-5491.2011.03246.x
    Article CAS PubMed Google Scholar
30. Poff AM, Rho JM, D'Agostino DP (2019) Ketone administration for seizure disorders: history and rationale for ketone esters and metabolic alternatives. Front Neurosci 13:1041. https://doi.org/10.3389/fnins.2019.01041
    Article PubMed PubMed Central Google Scholar
31. Randle PJ, England PJ, Denton RM (1970) Control of the tricarboxylate cycle and its interactions with glycolysis during acetate utilization in rat heart. Biochem J 117(4):677–695. https://doi.org/10.1042/bj1170677
    Article CAS PubMed PubMed Central Google Scholar
32. Klement RJ (2017) Beneficial effects of ketogenic diets for cancer patients: a realist review with focus on evidence and confirmation. Med Oncol 34(8):132. https://doi.org/10.1007/s12032-017-0991-5
    Article PubMed Google Scholar
33. Weber DD, Aminazdeh-Gohari S, Kofler B (2018) Ketogenic diet in cancer therapy. Aging (Albany NY) 10(2):164–165. https://doi.org/10.18632/aging.101382
    Article Google Scholar
34. Champ CE, Palmer JD, Volek JS, Werner-Wasik M, Andrews DW, Evans JJ, Glass J, Kim L, Shi W (2014) Targeting metabolism with a ketogenic diet during the treatment of glioblastoma multiforme. J Neurooncol 117(1):125–131. https://doi.org/10.1007/s11060-014-1362-0
    Article CAS PubMed Google Scholar
35. Poff AM, Ari C, Arnold P, Seyfried TN, D'Agostino DP (2014) Ketone supplementation decreases tumor cell viability and prolongs survival of mice with metastatic cancer. Int J Cancer 135(7):1711–1720. https://doi.org/10.1002/ijc.28809
    Article CAS PubMed PubMed Central Google Scholar
36. Liu H, Kurtoglu M, Leon-Annicchiarico CL, Munoz-Pinedo C, Barredo J, Leclerc G, Merchan J, Liu X, Lampidis TJ (2016) Combining 2-deoxy-D-glucose with fenofibrate leads to tumor cell death mediated by simultaneous induction of energy and ER stress. Oncotarget 7(24):36461–36473. https://doi.org/10.18632/oncotarget.9263
    Article PubMed PubMed Central Google Scholar
37. Stein M, Lin H, Jeyamohan C, Dvorzhinski D, Gounder M, Bray K, Eddy S, Goodin S, White E, Dipaola RS (2010) Targeting tumor metabolism with 2-deoxyglucose in patients with castrate-resistant prostate cancer and advanced malignancies. Prostate 70(13):1388–1394. https://doi.org/10.1002/pros.21172
    Article CAS PubMed PubMed Central Google Scholar
38. Raez LE, Papadopoulos K, Ricart AD, Chiorean EG, Dipaola RS, Stein MN, Rocha Lima CM, Schlesselman JJ, Tolba K, Langmuir VK, Kroll S, Jung DT, Kurtoglu M, Rosenblatt J, Lampidis TJ (2013) A phase I dose-escalation trial of 2-deoxy-D-glucose alone or combined with docetaxel in patients with advanced solid tumors. Cancer Chemother Pharmacol 71(2):523–530. https://doi.org/10.1007/s00280-012-2045-1
    Article CAS PubMed Google Scholar
39. Voss M, Lorenz NI, Luger AL, Steinbach JP, Rieger J, Ronellenfitsch MW (2018) Rescue of 2-deoxyglucose side effects by ketogenic diet. Int J Mol Sci. https://doi.org/10.3390/ijms19082462
    Article PubMed PubMed Central Google Scholar
40. Shukla SK, Gebregiworgis T, Purohit V, Chaika NV, Gunda V, Radhakrishnan P, Mehla K, Pipinos II, Powers R, Yu F, Singh PK (2014) Metabolic reprogramming induced by ketone bodies diminishes pancreatic cancer cachexia. Cancer Metab 2:18. https://doi.org/10.1186/2049-3002-2-18
    Article PubMed PubMed Central Google Scholar
41. Du X, Shi Z, Peng Z, Zhao C, Zhang Y, Wang Z, Li X, Liu G, Li X (2017) Acetoacetate induces hepatocytes apoptosis by the ROS-mediated MAPKs pathway in ketotic cows. J Cell Physiol 232(12):3296–3308. https://doi.org/10.1002/jcp.25773
    Article CAS PubMed Google Scholar
42. Fine EJ, Miller A, Quadros EV, Sequeira JM, Feinman RD (2009) Acetoacetate reduces growth and ATP concentration in cancer cell lines which over-express uncoupling protein 2. Cancer Cell Int 9:14. https://doi.org/10.1186/1475-2867-9-14
    Article CAS PubMed PubMed Central Google Scholar
43. Sreedhar A, Petruska P, Miriyala S, Panchatcharam M, Zhao Y (2017) UCP2 overexpression enhanced glycolysis via activation of PFKFB2 during skin cell transformation. Oncotarget 8(56):95504–95515. https://doi.org/10.18632/oncotarget.20762
    Article PubMed PubMed Central Google Scholar
44. Marsh J, Mukherjee P, Seyfried TN (2008) Drug/diet synergy for managing malignant astrocytoma in mice: 2-deoxy-D-glucose and the restricted ketogenic diet. Nutr Metab (Lond) 5:33. https://doi.org/10.1186/1743-7075-5-33
    Article CAS Google Scholar

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