Loss of the tumor suppressor Hace1 leads to ROS-dependent glutamine addiction

Oncogene

Volumn 34, Issue 30, 2015, Pages 4005-4010

  Cetinbas, N ^a,b   Daugaard, M ^a,b   Mullen, A R ^a,b   Hajee, S ^a   Rotblat, B ^a,b,c   Lopez, A ^a   Li, A ^a   DeBerardinis, R J ^a,b   Sorensen, P H ^a,b  

^a BRITISH COLUMBIA CANCER RESEARCH CENTRE   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; AMMONIA; CARBON; GLUTAMINE; GUANOSINE TRIPHOSPHATASE; HECT DOMAIN AND ANKYRIN REPEAT CONTAINING E3 UBIQUITINPROTEIN LIGASE 1; OXALOACETIC ACID; RAC1 PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; HACE1 PROTEIN, MOUSE; UBIQUITIN PROTEIN LIGASE;

AMINO ACID METABOLISM; ANIMAL CELL; ARTICLE; CELL DEATH; CITRIC ACID CYCLE; COLONY FORMATION; CONTROLLED STUDY; GENE INACTIVATION; HEK293 CELL LINE; HUMAN; HUMAN CELL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; WILD TYPE; ANIMAL; APOPTOSIS; CELL CULTURE; GENETICS; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY;

MUS;

ANIMALS; APOPTOSIS; CELLS, CULTURED; GLUTAMINE; MICE, KNOCKOUT; REACTIVE OXYGEN SPECIES; TUMOR SUPPRESSOR PROTEINS; UBIQUITIN-PROTEIN LIGASES;

EID: 84937968917     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2014.316     Document Type: Article

References (39)

1. Anglesio MS, Evdokimova V, Melnyk N, Zhang L, Fernandez CV, Grundy PE et al. Differential expression of a novel ankyrin containing E3 ubiquitin-protein ligase, Hace1, in sporadic Wilms' tumor versus normal kidney. Hum Mol Genet 2004; 13: 2061-2074.
2. Zhang L, Anglesio MS, O'Sullivan M, Zhang F, Yang G, Sarao R et al. The E3 ligase HACE1 is a critical chromosome 6q21 tumor suppressor involved in multiple cancers. Nat Med 2007; 13: 1060-1069.
3. Hibi K, Sakata M, Sakuraba K, Shirahata A, Goto T, Mizukami H et al. Aberrant methylation of the HACE1 gene is frequently detected in advanced colorectal cancer. Anticancer Res 2008; 28: 1581-1584.
4. Thelander EF, Ichimura K, Corcoran M, Barbany G, Nordgren A, Heyman M et al. Characterization of 6q deletions in mature B cell lymphomas and childhood acute lymphoblastic leukemia. Leuk Lymphoma 2008; 49: 477-487.
5. Sakata M, Kitamura YH, Sakuraba K, Goto T, Mizukami H, Saito M et al. Methylation of HACE1 in gastric carcinoma. Anticancer Res 2009; 29: 2231-2233.
6. Huang Y, de Reynies A, de Leval L, Ghazi B, Martin-Garcia N, Travert M et al. Gene expression profiling identifies emerging oncogenic pathways operating in extranodal NK/T-cell lymphoma, nasal type. Blood 2010; 115: 1226-1237.
7. Slade I, Stephens P, Douglas J, Barker K, Stebbings L, Abbaszadeh F et al. Constitutional translocation breakpoint mapping by genome-wide paired-end sequencing identifies HACE1 as a putative Wilms tumour susceptibility gene. J Med Genet 2010; 47: 342-347.
8. Diskin SJ, Capasso M, Schnepp RW, Cole KA, Attiyeh EF, Hou C et al. Common variation at 6q16 within HACE1 and LIN28B influences susceptibility to neuroblastoma. Nat Genet 2012; 44: 1126-1130.
9. Torrino S, Visvikis O, Doye A, Boyer L, Stefani C, Munro P et al. The E3 ubiquitinligase HACE1 catalyzes the ubiquitylation of active Rac1. Dev Cell 2011; 21: 959-965.
10. Castillo-Lluva S, Tan CT, Daugaard M, Sorensen PH, Malliri A. The tumour suppressor HACE1 controls cell migration by regulating Rac1 degradation. Oncogene 2013; 32: 1735-1742.
11. Cheng G, Diebold BA, Hughes Y, Lambeth JD. Nox1-dependent reactive oxygen generation is regulated by Rac1. J Biol Chem 2006; 281: 17718-17726.
12. Ueyama T, Geiszt M, Leto TL. Involvement of Rac1 in activation of multicomponent Nox1-and Nox3-based NADPH oxidases. Mol Cell Biol 2006; 26: 2160-2174.
13. Daugaard M, Nitsch R, Razaghi B, McDonald L, Jarrar A, Torrino S et al. Hace1 controls ROS generation of vertebrate Rac1-dependent NADPH oxidase complexes. Nat Commun 2013; 4: 2180.
14. Rotblat B, Southwell AL, Ehrnhoefer DE, Skotte NH, Metzler M, Franciosi S et al. HACE1 reduces oxidative stress and mutant Huntingtin toxicity by promoting the NRF2 response. Proc Natl Acad Sci USA 2014; 111: 3032-3037.
15. Cantor JR, Sabatini DM. Cancer cell metabolism: one hallmark, many faces. Cancer Discov 2012; 2: 881-898.
16. DeBerardinis RJ. Is cancer a disease of abnormal cellular metabolism? New angles on an old idea. Genet Med 2008; 10: 767-777.
17. Deberardinis RJ, Sayed N, Ditsworth D, Thompson CB. Brick by brick: metabolism and tumor cell growth. Curr Opin Genet Dev 2008; 18: 54-61.
18. DeBerardinis RJ, Lum JJ, Hatzivassiliou G, Thompson CB. The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metab 2008; 7: 11-20.
19. Klimberg VS, McClellan JL. Claude H. Organ Jr. Honorary Lectureship. Glutamine, cancer, and its therapy. Am J Surg 1996; 172: 418-424.
20. Rajagopalan KN, DeBerardinis RJ. Role of glutamine in cancer: Therapeutic and imaging implications. J Nucl Med. 2011; 52: 1005-1008.
21. Wise DR, Thompson CB. Glutamine addiction: A new therapeutic target in cancer. Trends Biochem Sci 2010; 35: 427-433.
22. Wise DR, DeBerardinis RJ, Mancuso A, Sayed N, Zhang XY, Pfeiffer HK et al. Myc regulates a transcriptional program that stimulates mitochondrial glutaminolysis and leads to glutamine addiction. Proc Natl Acad Sci USA 2008; 105: 18782-18787.
23. Gao P, Tchernyshyov I, Chang TC, Lee YS, Kita K, Ochi T et al. c-Myc suppression of miR-23a/b enhances mitochondrial glutaminase expression and glutamine metabolism. Nature 2009; 458: 762-765.
24. Weinberg F, Hamanaka R, Wheaton WW, Weinberg S, Joseph J, Lopez M et al. Mitochondrial metabolism and ROS generation are essential for Kras-mediated tumorigenicity. Proc Natl Acad Sci USA 2010; 107: 8788-8793.
25. Reynolds MR, Lane AN, Robertson B, Kemp S, Liu Y, Hill BG et al. Control of glutamine metabolism by the tumor suppressor Rb. Oncogene 2013; 33: 556-566.
26. Nicolay BN, Gameiro PA, Tschop K, Korenjak M, Heilmann AM, Asara JM et al. Loss of RBF1 changes glutamine catabolism. Genes Dev 2013; 27: 182-196.
27. Shanware NP, Mullen AR, DeBerardinis RJ, Abraham RT. Glutamine: pleiotropic roles in tumor growth and stress resistance. J Mol Med (Berl) 2011; 89: 229-236.
28. DeBerardinis RJ, Mancuso A, Daikhin E, Nissim I, Yudkoff M, Wehrli S et al. Beyond aerobic glycolysis: Transformed cells can engage in glutamine metabolism that exceeds the requirement for protein and nucleotide synthesis. Proc Natl Acad Sci USA 2007; 104: 19345-19350.
29. DeBerardinis RJ, Cheng T. Q's next: The diverse functions of glutamine in metabolism, cell biology and cancer. Oncogene 2010; 29: 313-324.
30. Fan J, Ye J, Kamphorst JJ, Shlomi T, Thompson CB, Rabinowitz JD. Quantitative flux analysis reveals folate-dependent NADPH production. Nature 2014; 510: 298-302.
31. Son J, Lyssiotis CA, Ying H, Wang X, Hua S, Ligorio M et al. Glutamine supports pancreatic cancer growth through a KRAS-regulated metabolic pathway. Nature 2013; 496: 101-105.
32. Wellen KE, Lu C, Mancuso A, Lemons JM, Ryczko M, Dennis JW et al. The hexosamine biosynthetic pathway couples growth factor-induced glutamine uptake to glucose metabolism. Genes Dev 2010; 24: 2784-2799.
33. Tong X, Zhao F, Thompson CB. The molecular determinants of de novo nucleotide biosynthesis in cancer cells. Curr Opin Genet Dev 2009; 19: 32-37.
34. Moldave K, Meister A. Synthesis of phenylacetylglutamine by human tissue. J Biol Chem 1957; 229: 463-476.
35. Li XN, Parikh S, Shu Q, Jung HL, Chow CW, Perlaky L et al. Phenylbutyrate and phenylacetate induce differentiation and inhibit proliferation of human medulloblastoma cells. Clin Cancer Res 2004; 10: 1150-1159.
36. Nicklin P, Bergman P, Zhang B, Triantafellow E, Wang H, Nyfeler B et al. Bidirectional transport of amino acids regulates mTOR and autophagy. Cell 2009; 136: 521-534.
37. Gianni D, Taulet N, Zhang H, DerMardirossian C, Kister J, Martinez L et al. A novel and specific NADPH oxidase-1 (Nox1) small-molecule inhibitor blocks the formation of functional invadopodia in human colon cancer cells. ACS Chem Biol 2010; 5: 981-993.
38. Cheng T, Sudderth J, Yang C, Mullen AR, Jin ES, Mates JM et al. Pyruvate carboxylase is required for glutamine-independent growth of tumor cells. Proc Natl Acad Sci USA 2011; 108: 8674-8679.
39. Fernandez CA, Des Rosiers C, Previs SF, David F, Brunengraber H. Correction of 13C mass isotopomer distributions for natural stable isotope abundance. J Mass Spectrom 1996; 31: 255-262.