Lactate dehydrogenase A silencing in IDH mutant gliomas

Neuro-Oncology

Volumn 16, Issue 5, 2014, Pages 686-695

  Chesnelong, Charles ^a,b   Chaumeil, Myriam M ^d   Blough, Michael D ^a,b   Al Najjar, Mohammad ^a,b   Stechishin, Owen D ^b,c   Chan, Jennifer A ^a,b   Pieper, Russell O ^e   Ronen, Sabrina M ^d   Weiss, Samuel ^a,b,c   Luchman, H Artee ^b,c   Cairncross, J Gregory ^a,b  

^a FOOTHILLS HOSPITAL   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c UNIVERSITY OF CALGARY   (Canada)

^d Southern Alberta Cancer Research Institute Health Research Innovation Centre ^*  (United States)

^e Brain Tumor Research Center   (United States)

Author keywords

Gliomas; Glycolysis; IDH mutation; LDHA; Methylation

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; ISOCITRATE DEHYDROGENASE; LACTATE DEHYDROGENASE; LACTATE DEHYDROGENASE ISOENZYME 5; PHOSPHOINOSITIDE DEPENDENT PROTEIN KINASE 1; UNCLASSIFIED DRUG; HIF1A PROTEIN, HUMAN; ISOENZYME; LACTATE DEHYDROGENASE 5;

ARTICLE; ASTROCYTE; BRAIN TUMOR; CANCER STEM CELL; CANCER TISSUE; CELL IMMORTALIZATION; CONTROLLED STUDY; DNA METHYLATION; ENZYME MECHANISM; GENE FREQUENCY; GENE MUTATION; GENE SILENCING; GENE TARGETING; GLIOBLASTOMA; GLYCOLYSIS; HUMAN; HUMAN CELL; HUMAN TISSUE; PROMOTER REGION; PROTEIN EXPRESSION; PYROSEQUENCING; TUMOR GENE; TUMOR XENOGRAFT; WILD TYPE; ANIMAL; BRAIN STEM TUMOR; GENE EXPRESSION REGULATION; GENETICS; GLIOMA; METABOLISM; MOUSE; MUTATION; TUMOR CELL LINE;

ANIMALS; BRAIN STEM NEOPLASMS; CELL LINE, TUMOR; DNA METHYLATION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; GLIOBLASTOMA; GLIOMA; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; ISOCITRATE DEHYDROGENASE; ISOENZYMES; L-LACTATE DEHYDROGENASE; MICE; MUTATION;

EID: 84899415660     PISSN: 15228517     EISSN: 15235866     Source Type: Journal    
DOI: 10.1093/neuonc/not243     Document Type: Article

References (40)

1. Yeung SJ Pan J Lee MH. Roles of p53 MYC and HIF-1 in regulating glycolysis-The seventh hallmark of cancer. Cell Mol Life Sci. 2008;65: 3981-3999
2. King A Selak MA Gottlieb E. Succinate dehydrogenase and fumarate hydratase: Linking mitochondrial dysfunction and cancer. Oncogene. 2006;25:4675-4682
3. Yan H Parsons DW Jin G et al. IDH1 and IDH2 mutations in gliomas. N Engl JMed. 2009;360:765-773
4. Parsons DW Jones S Zhang X et al. An integrated genomic analysis of human glioblastoma multiforme. Science. 2008;321:1807-1812
5. Yan H Bigner DD Velculescu V et al. Mutant metabolic enzymes are at the origin of gliomas. Cancer Res. 2009;69:9157-9159
6. KaelinWGJr. Cancer and altered metabolism: Potential importance of hypoxia-inducible factor and 2-oxoglutarate-dependent dioxygenases. Cold Spring Harb Symp Quant Biol. 2011;76:335-345
7. Dang L White DW Gross S et al. Cancer-Associated IDH1 mutations produce 2-hydroxyglutarate. Nature. 2009;462:739-744
8. Watanabe T Nobusawa S Kleihues P et al. IDH1 mutations are early events in the development of astrocytomas and oligodendrogliomas. Am J Pathol. 2009;174:1149-1153
9. GuoC Pirozzi CJ LopezGY et al. Isocitratedehydrogenasemutations in gliomas: Mechanisms biomarkers and therapeutic target. Curr Opin Neurol. 2011;24:648-652
10. Jin G Reitman ZJ Spasojevic I et al. 2-Hydroxyglutarate production but not dominant negative function is conferred by glioma-derived NADP-dependent isocitrate dehydrogenase mutations. PloS One. 2011;6:e16812
11. Xu W Yang H Liu Y et al. Oncometabolite 2-hydroxyglutarate is a competitive inhibitor of alpha-ketoglutarate-dependent dioxygenases. Cancer Cell. 2011;19:17-30
12. Chowdhury R Yeoh KK Tian YM et al. The oncometabolite 2-hydroxyglutarate inhibits histone lysine demethylases. EMBO Rep. 2011;12:463-469
13. Figueroa ME Abdel-Wahab O Lu C et al. Leukemic IDH1 and IDH2 mutations result in a hypermethylation phenotype disrupt TET2 function and impair hematopoietic differentiation. Cancer Cell. 2010; 18:553-567
14. He YF Li BZ Li Z et al. Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science. 2011;333: 1303-1307
15. Zhao S Lin Y XuW et al. Glioma-derivedmutations inIDH1 dominantly inhibit IDH1 catalytic activity and induce HIF-1alpha. Science. 2009; 324:261-265
16. Koivunen P Lee S Duncan CG et al. Transformation by the (R)-enantiomer of 2-hydroxyglutarate linked to EGLN activation. Nature. 2012;483:484-488
17. Baumgart E Fahimi HD Stich A et al. L-lactate dehydrogenase A4- And A3B isoforms are bona fide peroxisomal enzymes in rat liver: Evidence for involvement in intraperoxisomal NADH reoxidation. J Biol Chem. 1996;271:3846-3855
18. Rehse PH Davidson WS. Evolutionary relationship of a fish C-Type lactate-dehydrogenase to other vertebrate lactate-dehydrogenase isozymes. Can J Fish Aquat Sci. 1986;43:1045-1051
19. Walenta S Mueller-Klieser WF. Lactate: Mirror and motor of tumor malignancy. Semin Radiat Oncol. 2004;14:267-274
20. Goldman RD Kaplan NO Hall TC. Lactic dehydrogenase in human neoplastic tissues. Cancer Res. 1964;24:389-399
21. Firth JD Ebert BL Ratcliffe PJ. Hypoxic regulation of lactatedehydrogenase-A-interaction between hypoxia-inducible factor-1 and Camp response elements. J Biol Chem. 1995;270:21021-21027
22. Semenza GL Roth PH Fang HM et al. Transcriptional regulation of genes encoding glycolytic enzymes by hypoxia-inducible factor 1. J Biol Chem. 1994;269:23757-23763
23. Xie H Valera VA Merino MJ et al. LDH-A inhibition a therapeutic strategy for treatment of hereditary leiomyomatosis and renal cell cancer. Mol Cancer Ther. 2009;8:626-635
24. Le A Cooper CR Gouw AM et al. Inhibition of lactate dehydrogenase A induces oxidative stress and inhibits tumor progression. Proc Natl Acad Sci U S A. 2010;107:2037-2042
25. Fantin VR St-Pierre J Leder P. Attenuation of LDH-A expression uncovers a link between glycolysis mitochondrial physiology and tumor maintenance. Cancer Cell. 2006;9:425-434
26. Sheng SL Liu JJ Dai YH et al. Knockdown of lactate dehydrogenase A suppresses tumor growth and metastasis of human hepatocellular carcinoma. FEBS J. 2012;279:3898-3910
27. Yao F Zhao T Zhong C Zhu J Zhao H LDHA is necessary for the tumorigenicity of esophageal squamous cell carcinoma. Tumour Biol. 2013;34:25-31
28. Kelly JJ Stechishin O Chojnacki A et al. Proliferation of human glioblastoma stem cells occurs independently of exogenous mitogens. Stem Cells. 2009;27:1722-1733
29. Kelly JJ Blough MD Stechishin OD et al. Oligodendroglioma cell lines containing t(1;19)(q10;p10). Neuro-Oncology. 2010;12:745-755
30. Sonoda Y Ozawa T Hirose Y et al. Formation of intracranial tumors by genetically modified human astrocytes defines four pathways critical in the development of human anaplastic astrocytoma. Cancer Res. 2001;61:4956-4960
31. ChaumeilMMWoodsS DanforthRMet al. Non-invasiveassessment of IDH status in glioblastoma using dynamic 13C MRS of hyperpolarized a-ketoglutarate. Paper presented at: The 20th annual meeting of the International Society for Magnetic Resonance in Medicine 5-11 May 2012; Melbourne Australia
32. Brandes AH Ward CS Ronen SM. 17-Allyamino-17-demethoxygeldanamycin treatment results in a magnetic resonance spectroscopy-detectable elevation in choline-containing metabolites associated with increased expression of choline transporter SLC44A1 and phospholipase A2. Breast Cancer Res. 2010;12:R84
33. Rohle D Popovici-Muller J Palaskas N et al. Aninhibitor of mutant IDH1 delays growth and promotes differentiation of glioma cells. Science. 2013;340:626-630
34. TurcanSRohleDGoenkaAetal. IDH1mutationissufficient toestablish the glioma hypermethylator phenotype. Nature. 2012;483:479-483
35. Clark SJ Melki J.DNAmethylation andgene silencing in cancer: Which is the guilty party?. Oncogene. 2002;21:5380-5387
36. Turker MS. Gene silencing in mammalian cells and the spread of DNA methylation. Oncogene. 2002;21:5388-5393
37. Luo W Chang R Zhong J Pandey A Semenza G et al. Histone demethylase JMJD2C is a coactivator for hypoxia-inducible factor 1 that is required for breast cancer progression. Proc Natl Acad Sci USA. 2012. Dec 4;109(49):E3367-76
38. Houillier C Wang X Kaloshi G et al. IDH1 or IDH2 mutations predict longer survival and response to temozolomide in low-grade gliomas. Neurology. 2010;75:1560-1566
39. BloughMDAl-NajjarM ChesnelongC et al.DNAhypermethylationand 1p loss silence NHE-1 in oligodendroglioma. Ann Neurol. 2012;71: 845-849
40. Pouyssegur J Franchi A Pages G. pHi aerobic glycolysis and vascular endothelial growth factor in tumour growth. Novartis Found Symp. 2001;240:186-196; discussion 196-198.