Kidney-type glutaminase (GLS1) is a biomarker for pathologic diagnosis and prognosis of hepatocellular carcinoma

Oncotarget

Volumn 6, Issue 10, 2015, Pages 7619-7631

  Yu, Decai ^a   Shi, Xianbiao ^a   Meng, Gang ^a,b   Chen, Jun ^a   Yan, Chen ^c   Jiang, Yong ^c   Wei, Jiwu ^a,b   Ding, Yitao ^a  

^a MEDICAL SCHOOL OF NANJING UNIVERSITY   (China)

^b NANJING UNIVERSITY   (China)

^c THE THIRD AFFILIATED HOSPITAL OF SOOCHOW UNIVERSITY   (China)

Author keywords

Biomarker; Hepatocellular carcinoma; Kidney type glutaminase (GLS1); Liver type glutaminase (GLS2)

Indexed keywords

BIOLOGICAL MARKER; GLUTAMINASE; PROTEIN GLS1; PROTEIN GLS2; UNCLASSIFIED DRUG;

ADULT; ARTICLE; CANCER DIAGNOSIS; CANCER PROGNOSIS; CONTROLLED STUDY; DIAGNOSTIC TEST ACCURACY STUDY; FEMALE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; KIDNEY; LIVER CELL CARCINOMA; LIVER FIBROSIS; LIVER NODULE; MAJOR CLINICAL STUDY; MALE; PATHOLOGY; PROTEIN EXPRESSION; PROTEIN METABOLISM; RETROSPECTIVE STUDY; SENSITIVITY AND SPECIFICITY; SURVIVAL TIME; TUMOR GROWTH; GENETICS; LIVER TUMOR; METABOLISM; PROGNOSIS; TISSUE MICROARRAY; TUMOR CELL LINE;

BIOMARKERS; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; FEMALE; GLUTAMINASE; HUMANS; LIVER NEOPLASMS; MALE; PROGNOSIS; TISSUE ARRAY ANALYSIS;

EID: 84928408102     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3196     Document Type: Article

References (36)

1. Sakamoto M. Early, HCC: diagnosis and molecular markers. J Gastroenterol. 2009; 44:108-111.
2. Tremosini S, Forner A, Boix L, Vilana R, Bianchi L, Reig M, Rimola J, Rodriguez-Lope C, Ayuso C, Sole M, Bruix J. Prospective validation of an immunohistochemical panel (glypican 3, heat shock protein 70 and glutamine synthetase) in liver biopsies for diagnosis of very early hepatocellular carcinoma. Gut. 2012; 61:1481-1487.
3. Zhao Y, Butler EB, Tan M. Targeting cellular metabolism to improve cancer therapeutics. Cell Death Dis. 2013; 4:e532.
4. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011; 144:646-674.
5. Heiden MGV, Cantley LC, Thompson CB. Understanding the Warburg Effect: The Metabolic Requirements of Cell Proliferation. Science. 2009; 324:1029-1033.
6. DeBerardinis RJ, Mancuso A, Daikhin E, Nissim I, Yudkoff M, Wehrli S, Thompson CB. Beyond aerobic glycolysis: transformed cells can engage in glutamine metabolism that exceeds the requirement for protein and nucleotide synthesis. Proc Natl Acad Sci U S A. 2007; 104:19345-19350.
7. Zielke HR, Zielke CL, Ozand PT. Glutamine: a major energy source for cultured mammalian cells. Fed Proc. 1984; 43:121-125.
8. Matsuno T. Bioenergetics of tumor cells: glutamine metabolism in tumor cell mitochondria. Int J Biochem. 1987; 19:303-307.
9. Curthoys NP, Watford M. Regulation of glutaminase activity and glutamine metabolism. Annu Rev Nutr. 1995; 15:133-159.
10. DeBerardinis RJ, Cheng T. Q's next: the diverse functions of glutamine in metabolism, cell biology and cancer. Oncogene. 2010; 29:313-324.
11. Aledo JC, Gomez-Fabre PM, Olalla L, Marquez J. Identification of two human glutaminase loci and tissuespecific expression of the two related genes. Mamm Genome. 2000; 11:1107-1110.
12. Curthoys NP, Kuhlenschmidt T, Godfrey SS, Weiss RF. Phosphate-dependent glutaminase from rat kidney. Cause of increased activity in response to acidosis and identity with glutaminase from other tissues. Arch Biochem Biophys. 1976; 172:162-167.
13. Matés J, Segura J, Martín-Rufián M, Campos-Sandoval J, Alonso F, Márquez J. Glutaminase isoenzymes as key regulators in metabolic and oxidative stress against cancer. Curr Mol Med. 2013; 13:514-534.
14. Perez-Gomez C, Campos-Sandoval JA, Alonso FJ, Segura JA, Manzanares E, Ruiz-Sanchez P, Gonzalez ME, Marquez J, Mates JM. Co-expression of glutaminase K and L isoenzymes in human tumour cells. Biochem J. 2005; 386:535-542.
15. Szeliga M, Sidoryk M, Matyja E, Kowalczyk P, Albrecht J. Lack of expression of the liver-type glutaminase (LGA) mRNA in human malignant gliomas. Neurosci Lett. 2005; 374:171-173.
16. Szeliga M, Matyja E, Obara M, Grajkowska W, Czernicki T, Albrecht J. Relative expression of mRNAS coding for glutaminase isoforms in CNS tissues and CNS tumors. Neurochem Res. 2008; 33:808-813.
17. Turner A, McGivan JD. Glutaminase isoform expression in cell lines derived from human colorectal adenomas and carcinomas. Biochem J. 2003; 370:403-408.
18. Katunuma N, Kuroda Y, Sanada Y, Towatari T, Tomino I, Morris HP. Anomalous distribution of glutaminase isozyme in various hepatomas. Adv Enzyme Regul. 1970; 8:281-287.
19. Matsuno T, Satoh T. Glutamine metabolism in the avian host bearing transplantable hepatomatous growth induced by MC-29 virus. Int J Biochem. 1986; 18:187-189.
20. Matsuno T, Hirai H. Glutamine synthetase and glutaminase activities in various hepatoma cells. Biochem Int. 1989; 19:219-225.
21. Yuneva MO, Fan TW, Allen TD, Higashi RM, Ferraris DV, Tsukamoto T, Mates JM, Alonso FJ, Wang C, Seo Y, Chen X, Bishop JM. The metabolic profile of tumors depends on both the responsible genetic lesion and tissue type. Cell Metab. 2012; 15:157-170.
22. Dal Bello B, Rosa L, Campanini N, Tinelli C, Torello Viera F, D'Ambrosio G, Rossi S, Silini EM. Glutamine synthetase immunostaining correlates with pathologic features of hepatocellular carcinoma and better survival after radiofrequency thermal ablation. Clin Cancer Res. 2010; 16:2157-2166.
23. Cassago A, Ferreira AP, Ferreira IM, Fornezari C, Gomes ER, Greene KS, Pereira HM, Garratt RC, Dias SM, Ambrosio AL. Mitochondrial localization and structurebased phosphate activation mechanism of Glutaminase C with implications for cancer metabolism. Proc Natl Acad Sci U S A. 2012; 109:1092-1097.
24. Martin-Rufian M, Nascimento-Gomes R, Higuero A, Crisma AR, Campos-Sandoval JA, Gomez-Garcia MC, Cardona C, Cheng T, Lobo C, Segura JA, Alonso FJ, Szeliga M, Albrecht J, Curi R, Marquez J, Colquhoun A, Deberardinis RJ, Mates JM. Both GLS silencing and GLS2 overexpression synergize with oxidative stress against proliferation of glioma cells. J Mol Med (Berl). 2014; 92:277-290.
25. Wang JB, Erickson JW, Fuji R, Ramachandran S, Gao P, Dinavahi R, Wilson KF, Ambrosio AL, Dias SM, Dang CV, Cerione RA. Targeting mitochondrial glutaminase activity inhibits oncogenic transformation. Cancer Cell. 2010; 18:207-219.
26. Shukla K, Ferraris DV, Thomas AG, Stathis M, Duvall B, Delahanty G, Alt J, Rais R, Rojas C, Gao P, Xiang Y, Dang CV, Slusher BS, Tsukamoto T. 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. 2012; 55:10551-10563.
27. Meng G, Xia M, Xu C, Yuan D, Schnurr M, Wei J. Multifunctional antitumor molecule 5'-triphosphate siRNA combining glutaminase silencing and RIG-I activation. Int J Cancer. 2014; 134:1958-1971.
28. 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 ML, Shwonek PJ, Sjogren EB, Stanton TF, Wang T, Yang J, Zhao F, Bennett MK. Antitumor activity of the glutaminase inhibitor CB-839 in triple-negative breast cancer. Mol Cancer Ther. 2014; 13:890-901.
29. Liu J, Zhang C, Lin M, Zhu W, Liang Y, Hong X, Zhao Y, Young KH, Hu W and Feng Z. Glutaminase 2 negatively regulates the PI3K/AKT signaling and shows tumor suppression activity in human hepatocellular carcinoma. Oncotarget. 2014; 5:2635-2647.
30. Bruix J, Sherman M. Management of hepatocellular carcinoma. Hepatology. 2005; 42:1208-1236.
31. Wittekind C. Pitfalls in the classification of liver tumors. Pathologe. 2006; 27:289-293.
32. Bruix J, Sherman M. Management of hepatocellular carcinoma: an update. Hepatology. 2011; 53:1020-1022.
33. el-Assal ON, Yamanoi A, Soda Y, Yamaguchi M, Yu L, Nagasue N. Proposal of invasiveness score to predict recurrence and survival after curative hepatic resection for hepatocellular carcinoma. Surgery. 1997; 122:571-577.
34. Williams AR, Piris J, Wyllie AH. ras p21 expression in the progression of breast cancer. Hum Pathol. 1988; 19:1115.
35. Li Y, Tian B, Yang J, Zhao L, Wu X, Ye SL, Liu YK, Tang ZY. Stepwise metastatic human hepatocellular carcinoma cell model system with multiple metastatic potentials established through consecutive in vivo selection and studies on metastatic characteristics. J Cancer Res Clin Oncol. 2004; 130:460-468.
36. Yu D, Zhuang L, Sun X, Chen J, Yao Y, Meng K, Ding Y. Particular distribution and expression pattern of endoglin (CD105) in the liver of patients with hepatocellular carcinoma. BMC Cancer. 2007; 7:122.