L-asparaginase and inhibitors of glutamine synthetase disclose glutamine addiction of β-catenin-mutated human hepatocellular carcinoma cells

Current Cancer Drug Targets

Volumn 11, Issue 8, 2011, Pages 929-943

  Tardito, S ^a   Chiu, M ^a,b   Uggeri, J ^a   Zerbini, A ^c   Da Ros, F ^a   Dall'Asta, V ^a   Missale, G ^c   Bussolati, O ^a  

^a UNIVERSITY OF PARMA   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITY HOSPITAL OF PARMA   (Italy)

Author keywords

Cancer metabolism; Glutamine; Hepatocellular carcinoma; L asparaginase; catenin

Indexed keywords

2 OXOGLUTARIC ACID; AMINO ACID DERIVATIVE; ASPARAGINASE; BETA CATENIN; CARRIER PROTEIN; CASPASE 3; GLUTAMATE AMMONIA LIGASE; GLUTAMINE; INITIATION FACTOR 2ALPHA; MAMMALIAN TARGET OF RAPAMYCIN; METHIONINE SULFOXIMINE; PROTEIN KINASE B; PROTEIN SNAT2; PYRUVIC ACID; RAPAMYCIN; S6 KINASE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; AUTOPHAGY; BIOACCUMULATION; CANCER CELL CULTURE; CARCINOMA CELL; CELL PROLIFERATION; CELL STRAIN HEPG2; CONTROLLED STUDY; ENZYME INHIBITION; GENE MUTATION; HUMAN; HUMAN CELL; LIVER CELL CARCINOMA; ONCOGENE; PHENOTYPE; PROTEIN PHOSPHORYLATION; WILD TYPE;

EID: 80052854761     PISSN: 15680096     EISSN: 18735576     Source Type: Journal    
DOI: 10.2174/156800911797264725     Document Type: Article

References (48)

1. Bosch, F. X.; Ribes, J.; Cleries, R.; Diaz, M. Epidemiology of hepatocellular carcinoma. Clin. Liver Dis. 2005, 9 (2) 191-211, v.
2. Thompson, M. D.; Monga, S. P. WNT/beta-catenin signaling in liver health and disease. Hepatology 2007, 45 (5) 1298-1305.
3. Polakis, P. The many ways of Wnt in cancer. Curr. Opin. Genet. Dev. 2007, 17 (1), 45-51.
4. Hoppler, S.; Kavanagh, C. L. Wnt signalling: variety at the core. J. Cell Sci. 2007, 120 (Pt 3), 385-393.
5. Miyoshi, Y.; Iwao, K.; Nagasawa, Y.; Aihara, T.; Sasaki, Y.; Imaoka, S.; Murata, M.; Shimano, T.; Nakamura, Y. Activation of the betacatenin gene in primary hepatocellular carcinomas by somatic alterations involving exon 3. Cancer Res. 1998, 58 (12), 2524-2527.
6. Satoh, S.; Daigo, Y.; Furukawa, Y.; Kato, T.; Miwa, N.; Nishiwaki, T.; Kawasoe, T.; Ishiguro, H.; Fujita, M.; Tokino, T.; Sasaki, Y.; Imaoka, S.; Murata, M.; Shimano, T.; Yamaoka, Y.; Nakamura, Y. AXIN1 mutations in hepatocellular carcinomas, and growth suppression in cancer cells by virus-mediated transfer of AXIN1. Nat. Genet. 2000, 24 (3), 245-250.
7. Taniguchi, K.; Roberts, L. R.; Aderca, I. N.; Dong, X.; Qian, C.; Murphy, L. M.; Nagorney, D. M.; Burgart, L. J.; Roche, P. C.; Smith, D. I.; Ross, J. A.; Liu, W. Mutational spectrum of betacatenin, AXIN1, and AXIN2 in hepatocellular carcinomas and hepatoblastomas. Oncogene 2002, 21 (31), 4863-4871.
8. Lee, H. C.; Kim, M.; Wands, J. R. Wnt/Frizzled signaling in hepatocellular carcinoma. Front. Biosci. 2006, 11, 1901-1915.
9. Kim, M.; Lee, H. C.; Tsedensodnom, O.; Hartley, R.; Lim, Y. S.; Yu, E.; Merle, P.; Wands, J. R. Functional interaction between Wnt3 and Frizzled-7 leads to activation of the Wnt/beta-catenin signaling pathway in hepatocellular carcinoma cells. J. Hepatol. 2008, 48 (5), 780-791.
10. Cadoret, A.; Ovejero, C.; Terris, B.; Souil, E.; Levy, L.; Lamers, W. H.; Kitajewski, J.; Kahn, A.; Perret, C. New targets of betacatenin signaling in the liver are involved in the glutamine metabolism. Oncogene 2002, 21 (54), 8293-8301.
11. Dal Bello, B.; Rosa, L.; Campanini, N.; Tinelli, C.; Torello Viera, F.; D'Ambrosio, G.; Rossi, S.; Silini, E. M. Glutamine synthetase immunostaining correlates with pathologic features of hepatocellular carcinoma and better survival after radiofrequency thermal ablation. Clin. Cancer Res. 2010, 16 (7), 2157-2166.
12. Franchi-Gazzola, R.; Dall'Asta, V.; Sala, R.; Visigalli, R.; Bevilacqua, E.; Gaccioli, F.; Gazzola, G. C.; Bussolati, O. The role of the neutral amino acid transporter SNAT2 in cell volume regulation. Acta Physiol. (Oxf.) 2006, 187 (1-2), 273-283.
13. DeBerardinis, R. J.; Mancuso, A.; Daikhin, E.; Nissim, I.; Yudkoff, M.; Wehrli, S.; Thompson, C. B. 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 (49), 19345-19350.
14. Fumarola, C.; Zerbini, A.; Guidotti, G. G. Glutamine deprivationmediated cell shrinkage induces ligand-independent CD95 receptor signaling and apoptosis. Cell Death Differ. 2001, 8 (10), 1004-1013.
15. Lacoste, L.; Chaudhary, K. D.; Lapointe, J. Derepression of the glutamine synthetase in neuroblastoma cells at low concentrations of glutamine. J. Neurochem. 1982, 39 (1), 78-85.
16. Labow, B. I.; Souba, W. W.; Abcouwer, S. F. Mechanisms governing the expression of the enzymes of glutamine metabolism-glutaminase and glutamine synthetase. J. Nutr. 2001, 131 (9 Suppl), 2467S-74S; discussion 2486S-7S.
17. Haskell, C. M. L-Asparaginase: human toxicology and single agent activity in nonleukemic neoplasms. Cancer Treat Rep. 1981, 65 (Suppl 4), 57-59.
18. Verma, N.; Kumar, K.; Kaur, G.; Anand, S. L-asparaginase: a promising chemotherapeutic agent. Crit. Rev. Biotechnol. 2007, 27 (1), 45-62.
19. Tezuka, K.; Nakayama, H.; Honda, K.; Suzumiya, J.; Oshima, K.; Kitoh, T.; Ishii, E. Treatment of a child with myeloid/NK cell precursor acute leukemia with L-asparaginase and unrelated cord blood transplantation. Int. J. Hematol. 2002, 75 (2), 201-206.
20. Okada, S.; Hongo, T.; Yamada, S.; Watanabe, C.; Fujii, Y.; Ohzeki, T.; Horikoshi, Y.; Ito, T.; Yazaki, M.; Komada, Y.; Tawa, A. In vitro efficacy of l-asparaginase in childhood acute myeloid leukaemia. Br. J. Haematol. 2003, 123 (5), 802-809.
21. Ando, M.; Sugimoto, K.; Kitoh, T.; Sasaki, M.; Mukai, K.; Ando, J.; Egashira, M.; Schuster, S. M.; Oshimi, K. Selective apoptosis of natural killer-cell tumours by l-asparaginase. Br. J. Haematol. 2005, 130 (6), 860-868.
22. Yokoyama, H.; Yamamoto, J.; Tohmiya, Y.; Yamada, M. F.; Ohguchi, H.; Ohnishi, Y.; Okitsu, Y.; Fukuhara, N.; Ohba-Ohtsuka, R.; Kohata, K.; Ishizawa, K.; Kameoka, J.; Harigae, H. Allogeneic hematopoietic stem cell transplant following chemotherapy containing l-asparaginase as a promising treatment for patients with relapsed or refractory extranodal natural killer/T cell lymphoma, nasal type. Leuk. Lymphoma. 2010, 51, 1509-1512.
23. Lorenzi, P. L.; Reinhold, W. C.; Rudelius, M.; Gunsior, M.; Shankavaram, U.; Bussey, K. J.; Scherf, U.; Eichler, G. S.; Martin, S. E.; Chin, K.; Gray, J. W.; Kohn, E. C.; Horak, I. D.; Von Hoff, D. D.; Raffeld, M.; Goldsmith, P. K.; Caplen, N. J.; Weinstein, J. N. Asparagine synthetase as a causal, predictive biomarker for Lasparaginase activity in ovarian cancer cells. Mol. Cancer Ther. 2006, 5 (11), 2613-2623.
24. Lorenzi, P. L.; Weinstein, J. N. Asparagine synthetase: A new potential biomarker in ovarian cancer. Drug News Perspect. 2009, 22 (1), 61-64.
25. Lazarus, H.; McCoy, T. A.; Farber, S.; Barell, E. F.; Foley, G. E. Nutritional requirements of human leukemic cells. Asparagine requirements and the effect of L-asparaginase. Exp. Cell Res. 1969, 57 (1), 134-138.
26. Muller, H. J.; Boos, J. Use of L-asparaginase in childhood ALL. Crit. Rev. Oncol. Hematol. 1998, 28 (2), 97-113.
27. Bussolati, O.; Belletti, S.; Uggeri, J.; Gatti, R.; Orlandini, G.; Dall'Asta, V.; Gazzola, G. C. Characterization of apoptotic phenomena induced by treatment with L-asparaginase in NIH3T3 cells. Exp. Cell Res. 1995, 220 (2), 283-291.
28. Ollenschlager, G.; Roth, E.; Linkesch, W.; Jansen, S.; Simmel, A.; Modder, B. Asparaginase-induced derangements of glutamine metabolism: the pathogenetic basis for some drug-related sideeffects. Eur. J. Clin. Invest. 1988, 18 (5), 512-516.
29. Reinert, R. B.; Oberle, L. M.; Wek, S. A.; Bunpo, P.; Wang, X. P.; Mileva, I.; Goodwin, L. O.; Aldrich, C. J.; Durden, D. L.; McNurlan, M. A.; Wek, R. C.; Anthony, T. G. Role of glutamine depletion in directing tissue-specific nutrient stress responses to Lasparaginase. J. Biol. Chem. 2006, 281 (42), 31222-31233.
30. Rotoli, B. M.; Uggeri, J.; Dall'Asta, V.; Visigalli, R.; Barilli, A.; Gatti, R.; Orlandini, G.; Gazzola, G. C.; Bussolati, O. Inhibition of glutamine synthetase triggers apoptosis in asparaginase-resistant cells. Cell Physiol. Biochem. 2005, 15 (6), 281-292.
31. Tardito, S.; Uggeri, J.; Bozzetti, C.; Bianchi, M. G.; Rotoli, B. M.; Franchi-Gazzola, R.; Gazzola, G. C.; Gatti, R.; Bussolati, O. The inhibition of glutamine synthetase sensitizes human sarcoma cells to L-asparaginase. Cancer Chemother. Pharmacol. 2007, 60 (5), 751-758.
32. O'Brien, J.; Wilson, I.; Orton, T.; Pognan, F. Investigation of the Alamar Blue (resazurin) fluorescent dye for the assessment of mammalian cell cytotoxicity. Eur. J. Biochem. 2000, 267 (17), 5421-5426.
33. Minet, R.; Villie, F.; Marcollet, M.; Meynial-Denis, D.; Cynober, L. Measurement of glutamine synthetase activity in rat muscle by a colorimetric assay. Clin. Chim. Acta 1997, 268 (1-2), 121-132.
34. Bianchi, M. G.; Gazzola, G. C.; Tognazzi, L.; Bussolati, O. C6 glioma cells differentiated by retinoic acid overexpress the glutamate transporter excitatory amino acid carrier 1 (EAAC1). Neuroscience 2008, 151 (4), 1042-1052.
35. Bustin, S. A. Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. J. Mol. Endocrinol. 2000, 25 (2), 169-193.
36. Tardito, S.; Bussolati, O.; Gaccioli, F.; Gatti, R.; Guizzardi, S.; Uggeri, J.; Marchio, L.; Lanfranchi, M.; Franchi-Gazzola, R. Nonapoptotic programmed cell death induced by a copper(II) complex in human fibrosarcoma cells. Histochem. Cell Biol. 2006, 126 (4), 473-482.
37. Dall'Asta, V.; Bussolati, O.; Sala, R.; Parolari, A.; Alamanni, F.; Biglioli, P.; Gazzola, G. C. Amino acids are compatible osmolytes for volume recovery after hypertonic shrinkage in vascular endothelial cells. Am. J. Physiol. 1999, 276 (4 Pt 1), C865-C872.
38. Gazzola, G. C.; Dall'Asta, V.; Franchi-Gazzola, R.; White, M. F. The cluster-tray method for rapid measurement of solute fluxes in adherent cultured cells. Anal. Biochem. 1981, 115 (2), 368-374.
39. Cairo, S.; Armengol, C.; De Reynies, A.; Wei, Y.; Thomas, E.; Renard, C. A.; Goga, A.; Balakrishnan, A.; Semeraro, M.; Gresh, L.; Pontoglio, M.; Strick-Marchand, H.; Levillayer, F.; Nouet, Y.; Rickman, D.; Gauthier, F.; Branchereau, S.; Brugieres, L.; Laithier, V.; Bouvier, R.; Boman, F.; Basso, G.; Michiels, J. F.; Hofman, P.; Arbez-Gindre, F.; Jouan, H.; Rousselet-Chapeau, M. C.; Berrebi, D.; Marcellin, L.; Plenat, F.; Zachar, D.; Joubert, M.; Selves, J.; Pasquier, D.; Bioulac-Sage, P.; Grotzer, M.; Childs, M.; Fabre, M.; Buendia, M. A. Hepatic stem-like phenotype and interplay of Wnt/beta-catenin and Myc signaling in aggressive childhood liver cancer. Cancer Cell 2008, 14 (6), 471-484.
40. de La Coste, A.; Romagnolo, B.; Billuart, P.; Renard, C. A.; Buendia, M. A.; Soubrane, O.; Fabre, M.; Chelly, J.; Beldjord, C.; Kahn, A.; Perret, C. Somatic mutations of the beta-catenin gene are frequent in mouse and human hepatocellular carcinomas. Proc. Natl. Acad. Sci. U. S. A. 1998, 95 (15), 8847-8851.
41. Zeng, G.; Apte, U.; Cieply, B.; Singh, S.; Monga, S.P. SiRNAmediated beta-catenin knockdown in human hepatoma cells results in decreased growth and survival. Neoplasia 2007, 9 (11), 951-959.
42. Fenton, T. R.; Gout, I. T. Functions and regulation of the 70kDa ribosomal S6 kinases. Int. J. Biochem. Cell Biol. 2011, 43 (1), 47-59.
43. Tato, I.; Bartrons, R.; Ventura, F.; Rosa, J. L. Amino acids activate mammalian target of rapamycin complex 2 (mTORC2) via PI3K/Akt signaling. J. Biol. Chem. 2011, 286 (8), 6128-6142.
44. Mackenzie, B.; Erickson, J. D. Sodium-coupled neutral amino acid (System N/A) transporters of the SLC38 gene family. Pflugers Arch. 2004, 447 (5), 784-795.
45. Gazzola, R. F.; Sala, R.; Bussolati, O.; Visigalli, R.; Dall'Asta, V.; Ganapathy, V.; Gazzola, G. C. The adaptive regulation of amino acid transport system A is associated to changes in ATA2 expression. FEBS Lett. 2001, 490 (1-2), 11-14.
46. Cheng, T.; Sudderth, J.; Yang, C.; Mullen, A. R.; Jin, E. S.; Mates, J. M.; Deberardinis, R. J. Pyruvate carboxylase is required for glutamine-independent growth of tumor cells. Proc. Natl. Acad. Sci. U. S. A. 2011, 108 (21), 8674-8679.
47. Deberardinis, R. J.; Sayed, N.; Ditsworth, D.; Thompson, C. B. Brick by brick: metabolism and tumor cell growth. Curr. Opin. Genet. Dev. 2008, 18 (1), 54-61.
48. Tardito, S.; Chiu, M.; Franchi-Gazzola, R.; Dall'Asta, V.; Comi, P.; Bussolati, O. The non-proteinogenic amino acids L-methionine sulfoximine and DL-phosphinothricin activate mTOR. Amino Acids 2011, In press.