Opposing roles of glutaminase isoforms in determining glioblastoma cell phenotype

Neurochemistry International

Volumn 88, Issue , 2015, Pages 6-9

  Szeliga, Monika ^a   Albrecht, Jan ^a  

^a MOSSAKOWSKI MEDICAL RESEARCH CENTRE   (Poland)

Author keywords

Glioblastoma phenotype; GLS; GLS2

Indexed keywords

ALKYLATING AGENT; GLUTAMIC ACID; GLUTAMINASE; GLUTAMINE; PROTEIN P53; ISOENZYME;

ARTICLE; BRAIN TUMOR; CANCER GROWTH; CELL MIGRATION; CELL PROLIFERATION; GENE; GENE OVEREXPRESSION; GENE SILENCING; GLIOBLASTOMA; GLIOMA CELL; GLS GENE; GLS2 GENE; HUMAN; NONHUMAN; ONCOGENE C MYC; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; ENZYMOLOGY; GENETICS; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

ANIMALS; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; GLIOBLASTOMA; GLUTAMINASE; HUMANS; ISOENZYMES; PHENOTYPE;

EID: 84939574217     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2014.11.004     Document Type: Article

References (43)

1. J.C. Aledo, P.M. Gómez-Fabre, L. Olalla, and J. Márquez Identification of two human glutaminase loci and tissue-specific expression of the two related genes Mamm. Genome 11 2000 1107 1110
2. F. Ali-Osman, D.E. Stein, and A. Renwick Glutathione content and glutathione-5'-transferase expression in l,3-bis(2-chloroethyl)-l-nitrosourea-resistant human malignant astrocytoma cell lines Cancer Res 50 1990 6976 6980
3. Cheng T., J. Sudderth, Yang C., A.R. Mullen, Jin E.S., J.M. Matés, and et al. Pyruvate carboxylase is required for glutamine-independent growth of tumor cells Proc. Natl. Acad. Sci. U.S.A. 108 2011 8674 8679
4. N.P. Curthoys, and M. Watford Regulation of glutaminase activity and glutamine metabolism Annu. Rev. Nutr 15 1995 133 159
5. V. de la Rosa, J.A. Campos-Sandoval, M. Martín-Rufián, C. Cardona, J.M. Matés, J.A. Segura, and et al. A novel glutaminase isoform in mammalian tissues Neurochem. Int 55 2009 76 84
6. B. DeLaBarre, S. Gross, Fang C., Gao Y., A. Jha, Jiang F., and et al. Full-length human glutaminase in complex with an allosteric inhibitor Biochemistry 50 2011 10764 10770
7. A.C. Donadio, C. Lobo, M. Tosina, V. de la Rosa, M. Martín-Rufián, J.A. Campos-Sandoval, and et al. Antisense glutaminase inhibition modifies the O-GlcNAc pattern and flux through the hexosamine pathway in breast cancer cells J. Cell. Biochem 103 2008 800 811
8. K.M. Elgadi, R.A. Meguid, Qian M., W.W. Souba, and S.F. Abcouwer Cloning and analysis of unique human glutaminase isoforms generated by tissue-specific alternative splicing Physiol. Genomics 1 1999 51 62
9. A. Emadi, S.A. Jun, T. Tsukamoto, A.T. Fathi, M.D. Minden, and Dang C.V. Inhibition of glutaminase selectively suppresses the growth of primary acute myeloid leukemia cells with IDH mutations Exp. Hematol 42 2014 247 251
10. N.J. Ernest, and H. Sontheimer Extracellular glutamine is a critical modulator for regulatory volume increase in human glioma cells Brain Res 1144 2007 231 238
11. Gao P., I. Tchernyshyov, Chang T.C., Y.S. Lee, K. Kita, T. Ochi, and et al. c-Myc suppression of miR-23a/b enhances mitochondrial glutaminase expression and glutamine metabolism Nature 458 2009 762 765
12. P.M. Gomez-Fabre, J.C. Aledo, A. Del Castillo-Olivares, F.J. Alonso, I. Nunez De Castro, J.A. Campos, and et al. Molecular cloning, sequencing and expression studies of the human breast cancer cell glutaminase Biochem. J. 345 2000 365 375
13. Hu W., Zhang C., Wu R., Sun Y., A. Levine, and Feng Z. Glutaminase 2, a novel p53 target gene regulating energy metabolism and antioxidant function Proc. Natl. Acad. Sci. U.S.A. 107 2010 7455 7460
14. M. Iida, S. Sunaga, N. Hirota, N. Kuribayashi, H. Sakagami, M. Takeda, and et al. Effect of glutathione-modulating compounds on hydrogen-peroxide-induced cytotoxicity in human glioblastoma and glioma cell lines J. Cancer Res. Clin. Oncol 123 1997 619 622
15. F.V. Jacinto, and M. Esteller MGMT hypermethylation: a prognostic foe, a predictive friend DNA Repair (Amst) 6 2007 1155 1160
16. W.P. Katt, S. Ramachandran, J.W. Erickson, and R.A. Cerione Dibenzophenanthridines as inhibitors of glutaminase C and cancer cell proliferation Mol. Cancer Ther 11 2012 1269 1278
17. F. Lefranc, V. Facchini, and R. Kiss Proautophagic drugs: a novel means to combat apoptosis-resistant cancers, with a special emphasis on glioblastomas Oncologist 12 2007 1395 1403
18. C. Lobo, M.A. Ruiz-Bellido, J.C. Aledo, J. Márquez, I. De Castro Núñez, and F.J. Alonso Inhibition of glutaminase expression by antisense mRNA decreases growth and tumourigenicity of tumour cells Biochem. J. 348 2000 257 261
19. Lu J., Wang X.Y., and Tang W.H. Glutamine attenuates nitric oxide synthase expression and mitochondria membrane potential decrease in interleukin-1beta-activated rat hepatocytes Eur. J. Nutr 48 2009 333 339
20. J. Marquez, A.R. de la Oliva, J.M. Mates, J.A. Segura, and F.J. Alonso Glutaminase: a multifaceted protein not only involved in generating glutamate Neurochem. Int 8 2006 465 471
21. H. Ohgaki, and P. Kleihues Population-based studies on incidence, survival rates, and genetic alterations in astrocytic and oligodendroglial gliomas J. Neuropathol. Exp. Neurol 64 2005 479 489
22. H. Ohgaki, and P. Kleihues Genetic alterations and signaling pathways in the evolution of gliomas Cancer Sci 100 2009 2235 2241
23. L. Olalla, J.C. Aledo, G. Bannenberg, and J. Márquez The C-terminus of human glutaminase L mediates association with PDZ domain-containing proteins FEBS Lett 488 2001 116 122
24. L. Olalla, A. Gutiérrez, J.A. Campos, Z.U. Khan, F.J. Alonso, J.A. Segura, and et al. Nuclear localization of L-type glutaminase in mammalian brain J. Biol. Chem 277 2002 38939 38944
25. C. Pérez-Gómez, J.A. Campos-Sandoval, F.J. Alonso, J.A. Segura, E. Manzanares, P. Ruiz-Sánchez, and et al. Co-expression of glutaminase K and L isoenzymes in human tumour cells Biochem. J. 386 2005 535 542
26. A.E. Pegg, M.E. Dolan, and R.C. Moschel Structure, function and inhibition of O6-alkylguanine-DNA-alkyltransferase Prog. Nucleic Acid Res. Mol. Biol 51 1995 167 223
27. W.P. Roos, L.F. Batista, S.C. Naumann, W. Wick, M. Weller, C.F. Menck, and et al. Apoptosis in malignant glioma cells triggered by the temozolomide-induced DNA lesion O6-methylguanine Oncogene 26 2007 186 197
28. M.J. Seltzer, B.D. Bennett, A.D. Joshi, Gao P., A.G. Thomas, D.V. Ferraris, and et al. Inhibition of glutaminase preferentially slows growth of glioma cells with mutant IDH1 Cancer Res 70 2010 8981 8987
29. K. Shukla, D.V. Ferraris, A.G. Thomas, M. Stathis, B. Duvall, G. Delahanty, and et al. Design, synthesis, and pharmacological evaluation of bis-2-(5-phenylacetamido-1,2,4-thiadiazol-2-yl)ethyl sulfide 3 (BPTES) analogs as glutaminase inhibitors J. Med. Chem 55 2012 10551 10563
30. E.M. Smith, and M. Watford Molecular cloning of a cDNA for rat hepatic glutaminase. Sequence similarity to kidney-type glutaminase J. Biol. Chem 265 1990 10631 10636
31. H. Sontheimer A role for glutamate in growth and invasion of primary brain tumors J. Neurochem 105 2008 287 295
32. R. Stupp, W.P. Mason, M.J. van den Bent, M. Weller, B. Fisher, M.J. Taphoorn, and et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma N. Engl. J. Med 352 2005 987 996
33. S. Suzuki, T. Tanaka, M.V. Poyurovsky, H. Nagano, T. Mayama, S. Ohkubo, and et al. Phosphate-activated glutaminase (GLS2), a p53-inducible regulator of glutamine metabolism and reactive oxygen species Proc. Natl. Acad. Sci. U.S.A. 107 2010 7461 7466
34. M. Szeliga, and M. Obara-Michlewska Glutamine in neoplastic cells: focus on the expression and roles of glutaminases Neurochem. Int 55 2009 71 75
35. M. Szeliga, M. Sidoryk, E. Matyja, P. Kowalczyk, and J. Albrecht Lack of expression of the liver-type glutaminase (LGA) mRNA in human malignant gliomas Neurosci. Lett 374 2005 171 173
36. M. Szeliga, E. Matyja, M. Obara, W. Grajkowska, T. Czernicki, and J. Albrecht Relative expression of mRNAS coding for glutaminase isoforms in CNS tissues and CNS tumors Neurochem. Res 33 2008 808 813
37. M. Szeliga, M. Obara-Michlewska, E. Matyja, M. Łazarczyk, C. Lobo, W. Hilgier, and et al. Transfection with liver-type glutaminase cDNA alters gene expression and reduces survival, migration and proliferation of T98G glioma cells Glia 57 2009 1014 1023
38. M. Szeliga, A. Zgrzywa, M. Obara-Michlewska, and J. Albrecht Transfection of a human glioblastoma cell line with liver-type glutaminase (LGA) down-regulates the expression of DNA-repair gene MGMT and sensitizes the cells to alkylating agents J. Neurochem 123 2012 428 436
39. M. Szeliga, M. Bogacińska-Karaś, A. Rózycka, W. Hilgier, J. Marquez, and J. Albrecht Silencing of GLS and overexpression of GLS2 genes cooperate in decreasing the proliferation and viability of glioblastoma cells Tumour Biol 35 2014 1855 1862
40. A. Turner, and J.D. McGivan Glutaminase isoform expression in cell lines derived from human colorectal adenomas and carcinomas Biochem. J. 370 2003 403 408
41. Wang J.B., J.W. Erickson, R. Fuji, S. Ramachandran, Gao P., R. Dinavahi, and et al. Targeting mitochondrial glutaminase activity inhibits oncogenic transformation Cancer Cell 18 2010 207 219
42. M. Weller, S.M. Pfister, W. Wick, M.E. Hegi, G. Reifenberger, and R. Stupp Molecular neuro-oncology in clinical practice: a new horizon Lancet Oncol 14 2013 370 379
43. P.E. Wischmeyer Glutamine and heat shock protein expression Nutrition 18 2002 225 228