Arginine deiminase as a novel therapy for prostate cancer induces autophagy and caspase-independent apoptosis

Cancer Research

Volumn 69, Issue 2, 2009, Pages 700-708

  Kim, Randie H ^a   Coates, Jodi M ^a   Bowles, Tawnya L ^a   McNerney, Gregory P ^a   Sutcliffe, Julie ^a   Jung, Jae U ^b   Gandour Edwards, Regina ^a   Chuang, Frank Y S ^a   Bold, Richard J ^a,d   Kung, Hsing Jien ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; ARGININE DEIMINASE; ARGININOSUCCINATE SYNTHASE; BECLIN 1; CASPASE; CHLOROQUINE; DOCETAXEL; MACROGOL 20000; PEGYLATED ARGININE DEIMINASE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL DEATH; CELL STRAIN LNCAP; CONTROLLED STUDY; CORRELATION ANALYSIS; DRUG EFFICACY; ENZYME DEFICIENCY; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MICROARRAY ANALYSIS; MONOTHERAPY; MOUSE; NONHUMAN; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR GROWTH; TUMOR VOLUME; XENOGRAFT;

ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; ARGININOSUCCINATE SYNTHASE; AUTOPHAGY; CASPASE 3; CELL LINE, TUMOR; DRUG SYNERGISM; HUMANS; HYDROLASES; MALE; MICE; MICE, INBRED BALB C; MICE, NUDE; POLYETHYLENE GLYCOLS; PROSTATIC NEOPLASMS; TAXOIDS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 58349098150     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-08-3157     Document Type: Article

References (47)

1. Miyazaki K, Takaku H, Umeda M, et al. Potent growth inhibition of human tumor cells in culture by arginine deiminase purified from a culture medium of a Mycoplasma-infected cell line. Cancer Res 1990;50:4522-7.
2. Takaku H, Matsumoto M, Misawa S, Miyazaki K. Anti-tumor activity of arginine deiminase from Mycoplasma argini and its growth-inhibitory mechanism. Jpn J Cancer Res 1995;86:840-6.
3. Takaku H, Takase M, Abe S, Hayashi H, Miyazaki K. In vivo anti-tumor activity of arginine deiminase purified from Mycoplasma arginini. Int J Cancer 1992;51:244-9.
4. Ensor CM, Holtsberg FW, Bomalaski JS, Clark MA. Pegylated arginine deiminase (ADI-SS PEG20,000 mw) inhibits human melanomas and hepatocellular carcinomas in vitro and in vivo. Cancer Res 2002;62:5443-50.
5. Holtsberg FW, Ensor CM, Steiner MR, Bomalaski JS, Clark MA. Poly(ethylene glycol) (PEG) conjugated arginine deiminase: effects of PEG formulations on its pharmacological properties. J Control Release 2002;80:259-71.
6. Szlosarek PW, Klabatsa A, Pallaska A, 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;12:7126-31.
7. Yoon CY, Shim YJ, Kim EH, et al. Renal cell carcinoma does not express argininosuccinate synthetase and is highly sensitive to arginine deprivation via arginine deiminase. Int J Cancer 2007;120:897-905.
8. Bowles TL, Kim R, Galante J, et al. Pancreatic cancer cell lines deficient in argininosuccinate synthetase are sensitive to arginine deprivation by arginine deiminase. Int J Cancer 2008;123:1950-5.
9. Husson A, Brasse-Lagnel C, Fairand A, Renouf S, Lavoinne A. Argininosuccinate synthetase from the urea cycle to the citrulline-NO cycle. Eur J Biochem 2003;270:1887-99.
10. Lind DS. Arginine and cancer. J Nutr 2004;134:2837-41S; discussion 53S.
11. Shen LJ, Beloussow K, Shen WC. Modulation of arginine metabolic pathways as the potential anti-tumor mechanism of recombinant arginine deiminase. Cancer Lett 2006;231:30-5.
12. Dillon BJ, Prieto VG, Curley SA, et al. Incidence and distribution of argininosuccinate synthetase deficiency in human cancers: a method for identifying cancers sensitive to arginine deprivation. Cancer 2004;100:826-33.
13. Gong H, Zolzer F, von Recklinghausen G, et al. Arginine deiminase inhibits cell proliferation by arresting cell cycle and inducing apoptosis. Biochem Biophys Res Commun 1999;261:10-4.
14. Beloussow K, Wang L, Wu J, Ann D, Shen WC. Recombinant arginine deiminase as a potential antiangiogenic agent. Cancer Lett 2002;183:155-62.
15. Gong H, Pottgen C, Stuben G, Havers W, Stuschke M, Schweigerer L. Arginine deiminase and other antiangiogenic agents inhibit unfavorable neuroblastoma growth: potentiation by irradiation. Int J Cancer 2003;106:723-8.
16. Levine B, Klionsky DJ. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell 2004;6:463-77.
17. Mizushima N, Levine B, Cuervo AM, Klionsky DJ. Autophagy fights disease through cellular self-digestion. Nature 2008;451:1069-75.
18. Kabeya Y, Mizushima N, Ueno T, et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 2000;19:5720-8.
19. Mathew R, Karantza-Wadsworth V, White E. Role of autophagy in cancer. Nat Rev Cancer 2007;7:961-7.
20. Amaravadi RK, Thompson CB. The roles of therapy-induced autophagy and necrosis in cancer treatment. Clin Cancer Res 2007;13:7271-9.
21. Pattingre S, Espert L, Biard-Piechaczyk M, Codogno P. Regulation of macroautophagy by mTOR and Beclin 1 complexes. Biochimie 2008;90:313-23.
22. Maiuri MC, Criollo A, Tasdemir E, et al. BH3-only proteins and BH3 mimetics induce autophagy by competitively disrupting the interaction between Beclin 1 and Bcl-2/Bcl-X(L). Autophagy 2007;3:374-6.
23. Crighton D, Wilkinson S, O'Prey J, et al. DRAM, a p53-induced modulator of autophagy, is critical for apoptosis. Cell 2006;126:121-34.
24. Gozuacik D, Kimchi A. DAPk protein family and cancer. Autophagy 2006;2:74-9.
25. Desai SJ, Ma AH, Tepper CG, Chen HW, Kung HJ. Inappropriate activation of the androgen receptor by nonsteroids: involvement of the Src kinase pathway and its therapeutic implications. Cancer Res 2006;66:10449-59.
26. Parsons CM, Sutcliffe JL, Bold RJ. Preoperative evaluation of pancreatic adenocarcinoma. J Hepatobiliary Pancreat Surg 2008;15:429-35.
27. Van Poppel H. Recent docetaxel studies establish a new standard of care in hormone refractory prostate cancer. Can J Urol 2005;12 Suppl 1:81-5.
28. Mortimore GE, Schworer CM. Induction of autophagy by amino-acid deprivation in perfused rat liver. Nature 1977;270:174-6.
29. Liang C, Feng P, Ku B, et al. Autophagic and tumour suppressor activity of a novel Beclin1-binding protein UVRAG. Nat Cell Biol 2006;8:688-99.
30. Mizushima N, Yoshimori T. How to interpret LC3 immunoblotting. Autophagy 2007;3:542-5.
31. Codogno P, Meijer AJ. Autophagy and signaling: their role in cell survival and cell death. Cell Death Differ 2005;12 Suppl 2:1509-18.
32. Shinojima N, Yokoyama T, Kondo Y, Kondo S. Roles of the Akt/mTOR/p70S6K and ERK1/2 signaling pathways in curcumin-induced autophagy. Autophagy 2007;3:635-7.
33. Dillon BJ, Holtsberg FW, Ensor CM, Bomalaski JS, Clark MA. Biochemical characterization of the arginine degrading enzymes arginase and arginine deiminase and their effect on nitric oxide production. Med Sci Monit 2002;8:BR248-53.
34. Hardie DG. The AMP-activated protein kinase pathway-new players upstream and downstream. J Cell Sci 2004;117:5479-87.
35. Feun L, You M, Wu CJ, et al. Arginine deprivation as a targeted therapy for cancer. Curr Pharm Des 2008;14:1049-57.
36. Xu ZX, Liang J, Haridas V, et al. A plant triterpenoid, avicin D, induces autophagy by activation of AMP-activated protein kinase. Cell Death Differ 2007;14:1948-57.
37. Aoki H, Takada Y, Kondo S, Sawaya R, Aggarwal BB, Kondo Y. Evidence that curcumin suppresses the growth of malignant gliomas in vitro and in vivo through induction of autophagy: role of Akt and extracellular signal-regulated kinase signaling pathways. Mol Pharmacol 2007;72:29-39.
38. Pattingre S, Bauvy C, Codogno P. Amino acids interfere with the ERK1/2-dependent control of macroautophagy by controlling the activation of Raf-1 in human colon cancer HT-29 cells. J Biol Chem 2003;278:16667-74.
39. Maiuri MC, Zalckvar E, Kimchi A, Kroemer G. Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev 2007;8:741-52.
40. Maclean KH, Dorsey FC, Cleveland JL, Kastan MB. Targeting lysosomal degradation induces p53-dependent cell death and prevents cancer in mouse models of lymphomagenesis. J Clin Invest 2008;118:79-88.
41. Cheng PN, Lam TL, Lam WM, et al. Pegylated recombinant human arginase (rhArg-peg5,000mw) inhibits the in vitro and in vivo proliferation of human hepatocellular carcinoma through arginine depletion. Cancer Res 2007;67:309-17.
42. Xue LY, Chiu SM, Azizuddin K, Joseph S, Oleinick NL. Protection by Bcl-2 against apoptotic but not autophagic cell death after photodynamic therapy. Autophagy 2008;4:125-7.
43. Herman-Antosiewicz A, Johnson DE, Singh SV. Sulforaphane causes autophagy to inhibit release of cytochrome C and apoptosis in human prostate cancer cells. Cancer Res 2006;66:5828-35.
44. Cao C, Subhawong T, Albert JM, et al. Inhibition of mammalian target of rapamycin or apoptotic pathway induces autophagy and radiosensitizes PTEN null prostate cancer cells. Cancer Res 2006;66:10040-7.
45. Amaravadi RK, Yu D, Lum JJ, et al. Autophagy inhibition enhances therapy-induced apoptosis in a Myc-induced model of lymphoma. J Clin Invest 2007;117:326-36.
46. Izzo F, Marra P, Beneduce G, et al. Pegylated arginine deiminase treatment of patients with unresectable hepatocellular carcinoma: results from phase I/II studies. J Clin Oncol 2004;22:1815-22.
47. Ascierto PA, Scala S, Castello G, et al. Pegylated arginine deiminase treatment of patients with metastatic melanoma: results from phase I and II studies. J Clin Oncol 2005;23:7660-8.