A metabolic synthetic lethal strategy with arginine deprivation and chloroquine leads to cell death in ASS1-deficient sarcomas

Cell Death and Disease

Volumn 7, Issue 10, 2016, Pages

  Bean, Gregory R ^a   Kremer, Jeff C ^a   Prudner, Bethany C ^a   Schenone, Aaron D ^a   Yao, Juo Chin ^a   Schultze, Matthew B ^a   Chen, David Y ^a   Tanas, Munir R ^b   Adkins, Douglas R ^a,c   Bomalaski, John ^d   Rubin, Brian P ^b   Michel, Loren S ^a,c   Van Tine, Brian A ^a,c  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b LERNER RESEARCH INSTITUTE   (United States)

^c USA   (United States)

^d Polaris Group   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; ARGININOSUCCINATE SYNTHASE; ARGININOSUCCINATE SYNTHETASE 1; CHLOROQUINE; PEGARGIMINASE; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; HYDROLASE; MACROGOL DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; AUXOTROPHY; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; DRUG EFFICACY; GENE EXPRESSION; HISTOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; METABOLIC STRESS; MOUSE; NECROPTOSIS; NONHUMAN; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; SARCOMA; SARCOMA CELL LINE; AUTOPHAGY; CELL PROLIFERATION; DEFICIENCY; DRUG EFFECTS; DRUG RESISTANCE; ENZYMOLOGY; GENETICS; LETHAL MUTATION; METABOLISM; MOLECULARLY TARGETED THERAPY; NECROSIS; PATHOLOGY; TREATMENT OUTCOME; TUMOR CELL LINE;

ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; ARGININE; ARGININOSUCCINATE SYNTHASE; AUTOPHAGY; CELL LINE, TUMOR; CELL PROLIFERATION; CHLOROQUINE; DRUG RESISTANCE, NEOPLASM; HUMANS; HYDROLASES; MOLECULAR TARGETED THERAPY; NECROSIS; POLYETHYLENE GLYCOLS; PROGNOSIS; SARCOMA; SYNTHETIC LETHAL MUTATIONS; TREATMENT OUTCOME;

EID: 85010312669     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2016.232     Document Type: Article

References (43)

1. Taylor BS, Barretina J, Maki RG, Antonescu CR, Singer S, Ladanyi M. Advances in sarcoma genomics and new therapeutic targets. Nat Rev Cancer 2011; 11: 541–557.
2. Latres E, Drobnjak M, Pollack D, Oliva MR, Ramos M, Karpeh M et al. Chromosome 17 abnormalities and TP53 mutations in adult soft tissue sarcomas. Am J Pathol 1994; 145: 345–355.
3. Das P, Kotilingam D, Korchin B, Liu J, Yu D, Lazar AJ et al. High prevalence of p53 exon 4 mutations in soft tissue sarcoma. Cancer 2007; 109: 2323–2333.
4. Hoe KK, Verma CS, Lane DP. Drugging the p53 pathway: understanding the route to clinical efficacy. Nat Rev Drug Discov 2014; 13: 217–236.
5. Frith AE, Hirbe AC, Van Tine BA. Novel pathways and molecular targets for the treatment of sarcoma. Curr Oncol Rep 2013; 15: 378–385.
6. Cairns RA, Harris IS, Mak TW. Regulation of cancer cell metabolism. Nat Rev Cancer 2011; 11: 85–95.
7. Maki RG. Gemcitabine and docetaxel in metastatic sarcoma: past, present, and future. Oncologist 2007; 12: 999–1006.
8. Delage B, Fennell DA, Nicholson L, McNeish I, Lemoine NR, Crook T et al. Arginine deprivation and argininosuccinate synthetase expression in the treatment of cancer. Int J Cancer 2010; 126: 2762–2772.
9. Haines RJ, Pendleton LC, Eichler DC. Argininosuccinate synthase: at the center of arginine metabolism. Int J Biochem Mol Biol 2011; 2: 8–23.
10. Engel K, Hohne W, Haberle J. Mutations and polymorphisms in the human argininosuccinate synthetase (ASS1) gene. Hum Mutat 2009; 30: 300–307.
11. Qiu F, Chen Y-R, Liu X, Chu C-Y, Shen L-J, Xu J et al. Arginine starvation impairs mitochondrial respiratory function in ASS1-deficient breast cancer cells. Sci Signal 2014; 7: ra31–ra31.
12. Allen MD, Luong P, Hudson C, Leyton J, Delage B, Ghazaly E et al. Prognostic and therapeutic impact of argininosuccinate synthetase 1 control in bladder cancer as monitored longitudinally by PET imaging. Cancer Res 2014; 74: 896–907.
13. Kobayashi E, Masuda M, Nakayama R, Ichikawa H, Satow R, Shitashige M et al. Reduced argininosuccinate synthetase is a predictive biomarker for the development of pulmonary metastasis in patients with osteosarcoma. Mol Cancer Ther 2010; 9: 535–544.
14. Huang HY, Wu WR, Wang YH, Wang JW, Fang FM, Tsai JW et al. ASS1 as a novel tumor suppressor gene in myxofibrosarcomas: aberrant loss via epigenetic DNA methylation confers aggressive phenotypes, negative prognostic impact, and therapeutic relevance. Clin Cancer Res 2013; 19: 2861–2872.
15. Syed N, Langer J, Janczar K, Singh P, Lo Nigro C, Lattanzio L et al. Epigenetic status of argininosuccinate synthetase and argininosuccinate lyase modulates autophagy and cell death in glioblastoma. Cell Death Dis 2013; 4: e458.
16. Ott P, Carvajal R, Pandit-Taskar N, Jungbluth A, Hoffman E, Wu B-W et al. Phase I/II study of pegylated arginine deiminase (ADI-PEG 20) in patients with advanced melanoma. Invest New Drugs 2013; 31: 425–434.
17. Feun LG, Marini A, Walker G, Elgart G, Moffat F, Rodgers SE et al. Negative argininosuccinate synthetase expression in melanoma tumours may predict clinical benefit from arginine-depleting therapy with pegylated arginine deiminase. Br J Cancer 2012; 106: 1481–1485.
18. Kelly MP, Jungbluth AA, Wu BW, Bomalaski J, Old LJ, Ritter G. Arginine deiminase PEG20 inhibits growth of small cell lung cancers lacking expression of argininosuccinate synthetase. Br J Cancer 2012; 106: 324–332.
19. Yang TS, Lu SN, Chao Y, Sheen IS, Lin CC, Wang TE et al. A randomised phase II study of pegylated arginine deiminase (ADI-PEG 20) in Asian advanced hepatocellular carcinoma patients. Br J Cancer 2010; 103: 954–960.
20. Glazer ES, Piccirillo M, Albino V, Di Giacomo R, Palaia R, Mastro AA et al. Phase II study of pegylated arginine deiminase for nonresectable and metastatic hepatocellular carcinoma. J Clin Oncol 2010; 28: 2220–2226.
21. Bowles TL, Kim R, Galante J, Parsons CM, Virudachalam S, Kung H-J et al. Pancreatic cancer cell lines deficient in argininosuccinate synthetase are sensitive to arginine deprivation by arginine deiminase. Int J Cancer 2008; 123: 1950–1955.
22. Szlosarek PW, Klabatsa A, Pallaska A, Sheaff M, Smith P, Crook T et al. In vivo loss of expression of argininosuccinate synthetase in malignant pleural mesothelioma is a biomarker for susceptibility to arginine depletion. Clin Cancer Res 2006; 12: 7126–7131.
23. Szlosarek PW, Grimshaw MJ, Wilbanks GD, Hagemann T, Wilson JL, Burke F et al. Aberrant regulation of argininosuccinate synthetase by TNF-α in human epithelial ovarian cancer. Int J Cancer 2007; 121: 6–11.
24. Nicholson LJ, Smith PR, Hiller L, Szlosarek PW, Kimberley C, Sehouli J et al. Epigenetic silencing of argininosuccinate synthetase confers resistance to platinum-induced cell death but collateral sensitivity to arginine auxotrophy in ovarian cancer. Int J Cancer 2009; 125: 1454–1463.
25. You M, Savaraj N, Kuo M, Wangpaichitr M, Varona-Santos J, Wu C et al. TRAIL induces autophagic protein cleavage through caspase activation in melanoma cell lines under arginine deprivation. Mol Cell Biochem 2013; 374: 181–190.
26. Savaraj N, You M, Wu C, Wangpaichitr M, Kuo MT, Feun LG. Arginine deprivation, autophagy, apoptosis (AAA) for the treatment of melanoma. Curr Mol Med 2010; 10: 405–412.
27. Ju JS, Fuentealba RA, Miller SE, Jackson E, Piwnica-Worms D, Baloh RH et al. Valosin-containing protein (VCP) is required for autophagy and is disrupted in VCP disease. J Cell Biol 2009; 187: 875–888.
28. Mizushima N, Komatsu M. Autophagy: renovation of cells and tissues. Cell 2011; 147: 728–741.
29. Moscat J, Diaz-Meco MT. Feedback on fat: p62-mTORC1-autophagy connections. Cell 2011; 147: 724–727.
30. Feoktistova M, Leverkus M. Programmed necrosis and necroptosis signalling. FEBS J 2015; 282: 19–31.
31. Feoktistova M, Geserick P, Kellert B, Dimitrova Diana P, Langlais C, Hupe M et al. cIAPs block ripoptosome formation, a RIP1/caspase-8 containing intracellular cell death complex differentially regulated by cFLIP isoforms. Mol Cell 2011; 43: 449–463.
32. Radogna F, Dicato M, Diederich M. Cancer-type-specific crosstalk between autophagy, necroptosis and apoptosis as a pharmacological target. Biochem Pharmac 2015; 94: 1–11.
33. Feng S, Yang Y, Mei Y, Ma L, Zhu DE, Hoti N et al. Cleavage of RIP3 inactivates its caspase-independent apoptosis pathway by removal of kinase domain. Cell Signal 2007; 19: 2056–2067.
34. Ofengeim D, Yuan J. Regulation of RIP1 kinase signalling at the crossroads of inflammation and cell death. Nat Rev Mol Cell Biol 2013; 14: 727–736.
35. Nikoletopoulou V, Markaki M, Palikaras K, Tavernarakis N. Crosstalk between apoptosis, necrosis and autophagy. Biochim Biophys Acta 2013; 1833: 3448–3459.
36. Lin Y, Devin A, Rodriguez Y, Liu ZG. Cleavage of the death domain kinase RIP by caspase-8 prompts TNF-induced apoptosis. Genes Dev 1999; 13: 2514–2526.
37. Maycotte P, Aryal S, Cummings CT, Thorburn J, Morgan MJ, Thorburn A. Chloroquine sensitizes breast cancer cells to chemotherapy independent of autophagy. Autophagy 8: 200–212.
38. Bray K, Mathew R, Lau A, Kamphorst JJ, Fan J, Chen J et al. Autophagy suppresses RIP kinase-dependent necrosis enabling survival to mTOR inhibition. PloS One 2012; 7: e41831.
39. Yang S, Wang X, Contino G, Liesa M, Sahin E, Ying H et al. Pancreatic cancers require autophagy for tumor growth. Genes Dev 2011; 25: 717–729.
40. Shoushtari AN, Van Tine BA, Schwartz GK. Novel treatment targets in sarcoma: more than just the GIST, 2014/05/27 edn, 2014.
41. von Mehren M, Randall RL, Benjamin RS, Boles S, Bui MM, Casper ES et al. Soft tissue sarcoma, version 2.2014. J Natl Compr Cancer Network 2014; 12: 473–483.
42. Changou CA, Chen YR, Xing L, Yen Y, Chuang FY, Cheng RH et al. Arginine starvation-associated atypical cellular death involves mitochondrial dysfunction, nuclear DNA leakage, and chromatin autophagy. Proc Natl Acad Sci USA 2014; 111: 14147–14152.
43. Szlosarek PW. Arginine deprivation and autophagic cell death in cancer. Proc Natl Acad Sci USA 2014; 111: 14015–14016.