Enzymes in oncohematology: relevant directions of experimental studies and prospects of clinical use

V.S. Pokrovskiy, H.M. Treshchalina,

DOI:

https://doi.org/10.21320/2500-2139-2014-7-1-28-38

Recently, the field of development of the novel enzyme-based drugs showed remarkable advances. In addition to L-asparaginase which have been already used in oncohematology for more than 30 years, the two new enzymes, L-arginine deiminase and ranpirnase, underwent the several phases of clinical trials. Anticancer activity in vivo at the preclinical stage was shown for a number of enzymes: L-methionine-gamma-lyase, L-lysine-alpha-oxydase, and binase. This review discusses the enzymes which possess anticancer activity and prospects for their use in oncohematology.

  • V.S. Pokrovskiy N.N. Blokhin Russian Cancer Research Center of RAMS, Moscow, Russian Federation ; ФГБУ «Российский онкологический научный центр им. Н.Н. Блохина» РАМН, Москва, Российская Федерация
  • H.M. Treshchalina N.N. Blokhin Russian Cancer Research Center of RAMS, Moscow, Russian Federation ; ФГБУ «Российский онкологический научный центр им. Н.Н. Блохина» РАМН, Москва, Российская Федерация
  1. Kidd J.G. Regression of transplanted lymphomas induced in vivo by means of normal guinea pig serum. J. Exp. Med. 1953; 98: 565–82. DOI: https://doi.org/10.1084/jem.98.6.565
  2. Broome J.D. Evidence that the L-asparaginase activity of guinea pig serum is responsible for its antilymphoma effects. Nature 1961; 191: 1114–5. DOI: https://doi.org/10.1038/1911114a0
  3. Трещалина Е.М. Противоопухолевая активность веществ природного происхождения. М.: Практическая медицина, 2005. [Treshchalina Ye.M. Protivoopukholevaya aktivnost veshchestv prirodnogo proiskhozhdeniya (Anti-tumor activity of substances of natural origin). M.: Prakticheskaya meditsina, 2005.]
  4. Jaccard A., Petit B., Girault S. et al. L-asparaginase-based treatment of 15 western patients with extranodal NK/T-cell lymphoma and leukemia and a review of the literature. Ann Oncol. 2009; 20(1): 110–6. DOI: https://doi.org/10.1093/annonc/mdn542
  5. Obama K., Tara M., Niina K. L-asparaginase induced complete remission in Epstein-Barr virus positive, multidrug resistant, cutaneous T-cell lymphoma. Int. J. Hematol. 1999; 69(4): 260–2.
  6. Yong W., Zheng W., Zhang Y. et al. L-аsparaginase-based regimen in the treatment of refractory midline nasal/nasal-type T/NK-cell lymphoma. Int. J. Hematol. 2003; 78(2): 163–7. DOI: https://doi.org/10.1007/BF02983387
  7. Ollenschlager G., Roth E., Linkesch W. et al. Asparaginase-induced derangements of glutamine metabolism: the pathogenetic basis for some drugrelated side-effects. Eur. J. Clin Invest. 1988; 18(5): 512–6. DOI: https://doi.org/10.1111/j.1365-2362.1988.tb01049.x
  8. Villa P., Corada M., Bartosek I. L-asparaginase effects on inhibition of protein synthesis and lowering of the glutamine content in cultured rat hepatocytes. Toxicol. Lett. 1986; 32(3): 235–41. DOI: https://doi.org/10.1016/0378-4274(86)90113-X
  9. Warrell R.P.Jr., Chou T.C., Gordon C. et al. Phase I evaluation of succinylated Acinetobacter glutaminase-asparaginase in adults. Cancer Res. 1980; 40(12): 4546–51.
  10. Reinert R.B., Oberle L.M., Wek A.S. et al. Role of glutamine depletion in directing tissue-specific nutrient stress responses to L-asparagine. J. Biol. Chem. 2006; 281: 31222–33. DOI: https://doi.org/10.1074/jbc.M604511200
  11. Woods J.S., Handschumacher R.E. Hepatic homeostasis of plasma L-asparagine. Am. J. Physiol. 1971; 221: 1785–90. DOI: https://doi.org/10.1152/ajplegacy.1971.221.6.1785
  12. Bendich A., Kafkewitz D., Abuchowski A., Davis F.F. Immunological effects of native and polyethylene glycol-modified asparaginases from Vibrio succinogenes and Escherichia coli in normal and tumour-bearing mice. Clin. Exp. Immunol. 1982; 48: 273–8. DOI: https://doi.org/10.3109/08820138309050749
  13. Distasio J.A., Salazar A.M., Nadji M., Durden D.L. Glutaminase-free asparaginase from vibrio succinogenes: an antilymphoma enzyme lacking hepatotoxicity. Int. J. Cancer. 1982; 30(3): 343–7. DOI: https://doi.org/10.1002/ijc.2910300314
  14. Capizzy R.L., Cheng Y.C. Therapy of neoplasia with asparaginase. In: Enzymes as drug. Ed. by J.S. Holcenberg, J. Roberts. NY: John Wiley and Sons, 1981: 1–24.
  15. Storti E., Quaglino D. Dysmetabolic and neurological complications in leukemic patients treated with L-asparaginase. In: Experimental and clinical effects of L-asparaginase. Ed. by E. Grundmann, H.F. Oettgen. Berlin, Heidelberg, NY: Springer Verlag, 1970: 344–9. DOI: https://doi.org/10.1007/978-3-642-99984-0_40
  16. Roberts J., Schmid F.A., Old L.J., Stockert E. A comparative study of the antitumor effectiveness of E. coli and Erwinia asparaginases. Cancer Biochem. Biophys. 1976; 1(4): 175–8.
  17. Steiner M., Attarbaschi A., Kastner U. et al. Distinct fluctuations of ammonia levels during asparaginase therapy for childhood acute leukemia. Pediatr. Blood Cancer 2007; 9(5): 640–2. DOI: https://doi.org/10.1002/pbc.21022
  18. Watanabe S., Miyake K., Ogawa C. et al. The ex vivo production of ammonia predicts L-asparaginase biological activity in children with acute lymphoblastic leukemia. Int. J. Hematol. 2009; 90(3): 347–52. DOI: https://doi.org/10.1007/s12185-009-0419-x
  19. Гладилина Ю.А., Соколов Н.Н., Красоткина Ю.В. Клонирование, экспрессия и выделение L-аспарагиназы Helicobacter pylori. Биомед. хим. 2008; 54(4): С. 482–6. [Gladilina Yu.A., Sokolov N.N., Krasotkina Yu.V. Cloning, expression, and isolation of Helicobacter pylori L-asparaginase. Biomed. khim. 2008; 54(4): S. 482–6. (In Russ.)].
  20. Cappelletty D., Chiarelli L.R., Pasquetto M.V. et al. Helicobacter pylori L-asparaginase: A promising new chemotherapeutic agent. Biochem. Biophys. Res. Commun. 2008; 377: 1222–6. DOI: https://doi.org/10.1016/j.bbrc.2008.10.118
  21. Derst C., Henseling J., R hm K.H. Engineering the substrate specificity of Escherichia coli asparaginase II. Selective reduction of glutaminase activity by amino acid replacements at position 248. Protein Sci. 2000; 9: 2009–17. DOI: https://doi.org/10.1110/ps.9.10.2009
  22. Avramis V.I., Panosyan E.H. Pharmacokinetic/pharmacodynamic relationships of asparaginase formulations: the past, the present and recommendations for the future. Clin Pharmacokinet. 2005; 44: 367–93. DOI: https://doi.org/10.2165/00003088-200544040-00003
  23. Avramis V.I., Tiwari P.N. Asparaginase (native ASNase or pegylated ASNase) in the treatment of acute lymphoblastic leukemia. Int. J. Nanomed. 2006; 1(3): 241–54.
  24. Panosyan E.H., Grigoryan R.S., Avramis I.A. et al. Deamination of glutamine is a prerequisite for optimal asparagine deamination by asparaginases in vivo (CCG-1961). Anticancer Res. 2004; 24(2C): 1121–5.
  25. Rotoli B.M., Uggeri J., Dall’Asta V. et al. Inhibition of glutamine synthetase triggers apoptosis in asparaginase-resistant cells. Cell Physiol. Biochem. 2005; 15(6): 281–92. DOI: https://doi.org/10.1159/000087238
  26. Tardito S., Uggeri J., Bozzetto C. et al. The inhibition of glutamine synthetase sensitizes human sarcoma cells to L-asparaginase. Cancer Chemother. Pharmacol. 2007; 60(5): 751–8. DOI: https://doi.org/10.1007/s00280-007-0421-z
  27. Abuchowski A., Kazo G.M., Verhoest C.R. Jr. et al. Cancer therapy with chemically modified enzymes. I. Antitumor properties of polyethylene glycolasparaginase conjugates. Cancer Biochem. Biophys. 1984; 7(2): 175–86.
  28. Asselin B.L., Whitin J.C., Coppola D.J. et al. Comparative pharmacokinetic studies of three asparaginase preparations. J. Clin. Oncol. 1993; 11: 1780–6. 29. Khan A., Hill J.M. Atopic hypersensitivity to L-asparaginase: resistance to immunosupression. Int. Arch. Allergy Appl. Immunol. 1971; 40(3): 463–569. DOI: https://doi.org/10.1159/000230429
  29. Alvarez O.A., Zimmerman G. Pegaspargase-induced pancreatitis. Med. Pediatr. Oncol. 2000; 34(3): 200–5. DOI: https://doi.org/10.1002/(SICI)1096-911X(200003)34:3<200::AID-MPO7>3.0.CO;2-T
  30. Кучумова А.В., Красоткина Ю.В., Хасигов П.З., Соколов Н.Н. Пегили- рование рекомбинантной аспарагиназы Erwinia carotovora полиэтиленгликолем 5000. Биомед. хим. 2007; 53(1): 107–11. [Kuchumova A.V., Krasotkina Yu.V., Khasigov P.Z., Sokolov N.N. Pegylation of recombinant Erwinia carotovora asparaginase with polyethilenglycol. 5000. Biomed. khim. 2007; 53(1): 107–11. (In Russ.)]. DOI: https://doi.org/10.1134/S1990750807030092
  31. Gaspar M.M., Perez-Soler R., Cruz M.E. Biological characterization of L-asparaginase liposomal formulations. Cancer Chemother. Pharmacol. 1996; 38(4): 373–7. DOI: https://doi.org/10.1007/s002800050497
  32. Jean-Francois J., D’Urso E.M., Fortier G. Immobilization of L-asparaginase into a biocompatible poly(ethylene glycol)-albumin hydrogel: evaluation of performance in vivo. Biotechnol. Appl. Biochem. 1997; 26(Pt. 3): 203–12. DOI: https://doi.org/10.1111/j.1470-8744.1997.tb01332.x
  33. Gaspar M.M., Blanco D., Cruz M.E., Alonso M.J. Formulation of L-asparaginase load poly(lactide-to-glycolide) nanoparticles: influence of polymer properties on enzyme loading, activity and in vitro release. J. Control. Release 1998; 52: 53–62. DOI: https://doi.org/10.1016/S0168-3659(97)00196-X
  34. Qian G., Zhou J., Wang D., He B. The chemical modification of E. coli L-asparaginase by N, O-carboxymethyl chitosan. Artif. Cell. Blood Substit. Immobil. Biotechnol. 1996; 24: 567–77. DOI: https://doi.org/10.3109/10731199609118882
  35. Uren J.R., Hargis B.J., Beardsley P. Immunological and pharmacological characterization of poly-DL-alanyl-modified Erwinia carotovora L-asparaginase. Cancer Res. 1982; 42: 4068–71.
  36. Jorge J.C., Perez-Soler R., Morais J.G., Cruz M.E. Liposomal palmitoylL-asparaginase: characterization and biological activity. Cancer Chemother. Pharmacol. 1994; 34(3): 230–4. DOI: https://doi.org/10.1007/BF00685082
  37. Zhang Y.Q., Zhou W.L., Shen W.D. et al. Synthesis, characterization and immunogenicity of silk fibroin-L-asparaginase bioconjugates. J. Biotechnol. 2005; 120(3): 315–26. DOI: https://doi.org/10.1016/j.jbiotec.2005.06.027
  38. Leal-Egana A., Scheibel T. Silk-based materials for biomedical applications. Biotechnol. Appl. Biochem. 2010; 55(3): 155–67. DOI: https://doi.org/10.1042/BA20090229
  39. Spiess K., Lammel A., Scheibel T. Recombinant spider silk proteins for applications in biomaterials. Macromol. Biosci. 2010; 10(9): 998–1007. DOI: https://doi.org/10.1002/mabi.201000071
  40. Kwon Y.M., Chung H.S., Moon C. et al. L-Asparaginase encapsulated intact erythrocytes for treatment of acute lymphoblastic leukemia. J. Control. Release 2009; 139(3): 182–9. DOI: https://doi.org/10.1016/j.jconrel.2009.06.027
  41. Moola Z.B., Scawen M.D., Atkinson T., Nicholls D.J. Erwinia chrysanthemi L-asparaginase: epitope mapping and production of antigenically modified enzymes. Biochem. J. 1994; 302(Pt. 3): 921–7. DOI: https://doi.org/10.1042/bj3020921
  42. Goldberg A.I., Cooney D.A., Glynn J.P. et al. The effects of immunization to L-asparaginase on antitumor and enzymatic activity. Cancer Res. 1973; 33: 256–61.
  43. Vrooman L.M., Supko J.G., Neuberg D.S. et al. Erwinia asparaginase after allergy to E. coli asparaginase in children with acute lymphoblastic leukemia. Pediatr. Blood Cancer 2010; 54(2): 199–205. DOI: https://doi.org/10.1002/pbc.22225
  44. Zalewska-Szewczyk B., Gach A., Wyka K. et al. The cross-reactivity of anti-asparaginase antibodies against different L-asparaginase preparations. Clin. Exp. Med. 2009; 2: 113–6. DOI: https://doi.org/10.1007/s10238-008-0026-9
  45. Distasio J.A., Niederman R.A. Purification and characterization of Lasparaginase with anti-lymphoma activity from Vibrio succinogenes. J. Biol. Chem. 1976; 251(22): 6929–33. DOI: https://doi.org/10.1016/S0021-9258(17)32924-1
  46. Абакумова О.Ю., Подобед О.В., Борисова А.А. и др. Противоопухолевая активность L-аспарагиназы из Yersinia pseudotuberculosis. Биомед. хим. 2008; 54(6): 712–9. [Abakumova O.Yu., Podobed O.V., Borisova A.A. et al. Anti-tumor activity of Yersinia pseudotuberculosis L-asparaginase. Biomed. khim. 2008; 54(6): 712–9. (In Russ.)].
  47. Carta De-Angeli L., Pocchiari F. et al. Effect of L-asparaginase from Aspergillus terreus on ascites sarcoma in the rat. Nature (London) 1970; 225: 549–50. DOI: https://doi.org/10.1038/225549a0
  48. Peterson L.E., Ciegler A. L-asparaginase production by Erwinia aroideae. Appl. Microbiol. 1969; 18: 64–7. DOI: https://doi.org/10.1128/am.18.1.64-67.1969
  49. Pritsa A.A., Papazisis K.T., Kortsaris A.H. et al. Antitumor activity of Lasparaginase from Thermus thermophilus. Anticancer Drugs 2001; 12: 137–42. DOI: https://doi.org/10.1097/00001813-200102000-00007
  50. Reddy V.V.S., Jayaram H.N., Sirsi M., Ramakrishnan T. Inhibitory activity of L-asparaginase from Mycobacterium tuberculosis on Yoshida ascites sarcoma in rats. Arch. Biochem. Biophys. 1969; 132: 262–7. DOI: https://doi.org/10.1016/0003-9861(69)90361-0
  51. Rowley B., Wriston J.C. Partial purification and antilymphoma activity of Serratia marcescens L-asparaginase. Biochem. Biophys. Res. Commun. 1967; 28: 160–5. DOI: https://doi.org/10.1016/0006-291X(67)90423-8
  52. Pokrovskaya M.V., Pokrovsky V.S., Aleksandrova S.S. et al. Recombinant intracellular Rhodospirillum riubrum L-asparaginase with low L-glutaminase activity and antiproliferative effect. Biochem. (Mosc.). Suppl. Series B: Biomed. Chem. 2012; 6: 121–31. DOI: https://doi.org/10.1134/S1990750812020096
  53. Appel I.M., Hop W.C., Pieters R. Changes in hypercoagulability by asparaginase: a randomized study between two asparaginases. Blood Coagul. Fibrinol. 2006; 17: 139–46. DOI: https://doi.org/10.1097/01.mbc.0000214709.11492.ec
  54. Duval M., Suciu S., Ferster A. et al. Comparison of Escherichia coliasparaginase with Erwinia-asparaginase in the treatment of childhood lymphoid malignancies: results of a randomized European Organisation for Research and Treatment of Cancer-Children’s Leukemia Group phase 3 trial. Blood 2002; 99(8): 2734–9. DOI: https://doi.org/10.1182/blood.V99.8.2734
  55. Durden D.L., Salazar A.M., Distasio J.A. Kinetic analisys of hepatotoxicity associated with antineoplastic asparaginases. Cancer Res. 1983; 43: 1602–5.
  56. Eden O.B., Shaw M.P., Lilleyman J.S., Richards S. Non-randomised study comparing toxicity of Escherichia coli and Erwinia asparaginase in children with leukaemia. Med. Pediatr. Oncol. 1990; 18(6): 497–502. DOI: https://doi.org/10.1002/mpo.2950180612
  57. Howard J.B., Carpenter F.H. L-asparaginase from Erwinia carotovora. Substrate specificity and enzymatic properties. J. Biol. Chem. 1972; 247: 1020–30. DOI: https://doi.org/10.1016/S0021-9258(19)45610-X
  58. Bach S.J., Lasnitzki I. Some aspects of the role of arginine and arginase in mouse carcinoma 63. Enzymologia 1947; 12(3): 198–205.
  59. Bach S.J., Maw G.A. Creatine synthesis by tumor-bearing rats. Biochem. Biophys. Acta 1953; 11(1): 69–78. DOI: https://doi.org/10.1016/0006-3002(53)90009-2
  60. Osunkoya B.O., Adler W.H., Smith R.T. Effect of arginine deficiency on synthesis of DNA and immunoglobulin receptor of Burkitt lymphoma cells. Nature 1970; 227: 398–9. DOI: https://doi.org/10.1038/227398a0
  61. Storr J.M., Burton A.F. The effects of arginine deficiency on lymphoma cells. Br. J. Cancer 1974; 30: 50–9. DOI: https://doi.org/10.1038/bjc.1974.112
  62. Cheng P.N., Lam T.L., Lam W.M. et al. Pegylated recombinant human arginase inhibits the in vitro and in vivo proliferation of human hepatocellular carcinoma through arginine depletion. Cancer Res. 2007; 67(1): 309–17. DOI: https://doi.org/10.1158/0008-5472.CAN-06-1945
  63. Savoca K.V., Davis F.F., van Es T. et al. Cancer therapy with chemically modified enzymes. II. The therapeutic effectiveness of arginase, and arginase modified by the covalent attachment of polyethylene glycol, on the taper liver tumor and the L5178Y murine leukemia. Cancer Biochem. Biophys. 1984; 7(3): 261–8.
  64. Hernandez C.P., Morrow K., Lopez-Barcons L.A. et al. Pegylated arginase I: a potential therapeutic approach in T-ALL. Blood 2010; 115(25): 5214–21. DOI: https://doi.org/10.1182/blood-2009-12-258822
  65. Hsueh E.C., Knebel S.M., Lo W.H. et al. Deprivation of arginine by recombinant human arginase in prostate cancer cells. J. Hematol. Oncol. 2012; 5: 17. doi: 10.1186/1756-8722-5-17. DOI: https://doi.org/10.1186/1756-8722-5-17
  66. Shibatani T., Kakimoto T., Chibata I. Crystallization and properties of L-arginine deiminase of Pseudomonas putida. J. Biol. Chem. 1975; 250(12): 4580–3. DOI: https://doi.org/10.1016/S0021-9258(19)41341-0
  67. Takaku H., Takase M., Abe S. et al. In vivo anti-tumor activity of arginine deiminase purified from Mycoplasma arginini. Int. J. Cancer. 1992; 51(2): 244–9. DOI: https://doi.org/10.1002/ijc.2910510213
  68. Park I.S., Kang S.W., Shin Y.J. et al. Arginine deiminase: a potential inhibitor of angiogenesis and tumour growth. Br. J. Cancer 2003; 89: 907–14. DOI: https://doi.org/10.1038/sj.bjc.6601181
  69. Ni Y., Li Z., Sun Z. et al. Expression of arginine deiminase from Pseudomonas plecoglossicida CGMCC2039 in Escherichia coli and its anti-tumor activity. Curr. Microbiol. 2009; 58(6): 593–8. DOI: https://doi.org/10.1007/s00284-009-9376-0
  70. Ensor C.M., Holtsberg F.W., Bomalaski J.S., Clark M.A. 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.
  71. Gong H., Zolzer F., von Recklinghausen G. et al. Arginine deiminase inhibits proliferation of human leukemia cells more potently than asparaginase by inducing cell cycle arrest and apoptosis. Leukemia 2000; 14(5): 826–9. DOI: https://doi.org/10.1038/sj.leu.2401763
  72. Noh E.J., Kang S.W., Shin Y.J. et al. Arginine deiminase enhances dexamethasone-induced cytotoxicity in human T-lymphoblastic leukemia CCRF-CEM cells. Int. J. Cancer 2004: 112: 502–8. DOI: https://doi.org/10.1002/ijc.20435
  73. Ascierto P.A., 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. DOI: https://doi.org/10.1200/JCO.2005.02.0933
  74. Curley S.A., Bomalaski J.S., Ensor C.M. et al. Regression of hepatocellular cancer in a patient treated with arginine deiminase. Hepatogastroenterology 2003; 50(53): 1214–6.
  75. Glazer E.S., Piccirillo M., Albino V. et al. Phase II study of pegylated arginine deiminase for nonresectable and metastatic hepatocellular carcinoma. J. Clin. Oncol. 2010; 28(13): 2220–6. DOI: https://doi.org/10.1200/JCO.2009.26.7765
  76. 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. DOI: https://doi.org/10.1200/JCO.2004.11.120
  77. Glazer E.S., Piccirillo M., Albino V. et al. Phase II study of pegylated arginine deiminase for nonresectable and metastatic hepatocellular carcinoma. J. Clin. Oncol. 2010; 28(13): 2220–6. DOI: https://doi.org/10.1200/JCO.2009.26.7765
  78. Ott P.A., Carvajal R.D., Pandit-Taskar N. et al. Phase I/II study of pegylated arginine deiminase (ADI-PEG20) in patients with advanced melanoma. Invest. New Drugs 2013; 31(2): 425–34. DOI: https://doi.org/10.1007/s10637-012-9862-2
  79. Delage B., Luong P., Maharaj L. et al. Promoter methylation of argininosuccinate synthetase-1 sensitises lymphomas to arginine deiminase treatment, autophagy and caspase-dependent apoptosis. Cell Death Dis. 2012; 3: e342. DOI: https://doi.org/10.1038/cddis.2012.83
  80. Wu L., Li L., Meng S. et al. Expression of argininosuccinate synthetase in patients with hepatocellular carcinoma. J. Gastroenterol. Hepatol. 2013; 28(2): 365–8. DOI: https://doi.org/10.1111/jgh.12043
  81. Szlosarek P.W., Luong P., Phillips M.M. et al. Metabolic response to pegylated arginine deiminase in mesothelioma with promoter methylation of argininosuccinate synthetase. J. Clin. Oncol. 2013; 31(7): e111–3. DOI: https://doi.org/10.1200/JCO.2012.42.1784
  82. Feun L.G., Marini A., Walker G. 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(9): 1481–5. DOI: https://doi.org/10.1038/bjc.2012.106
  83. Kelly M.P., Jungbluth A.A., Wu B.W. et al. Arginine deiminase PEG20 inhibits growth of small cell lung cancers lacking expression of argininosuccinate synthetase. Br. J. Cancer 2012; 106(2): 324–32. DOI: https://doi.org/10.1038/bjc.2011.524
  84. Manca A., Sini M.C., Izzo F. et al. Induction of arginosuccinate synthetase (ASS) expression affects the antiproliferative activity of arginine deiminase (ADI) in melanoma cells. Oncol. Rep. 2011; 25(6): 1495–502.
  85. Bowles T.L., 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. DOI: https://doi.org/10.1002/ijc.23723
  86. Kim H.J., Kim J.H., Yu Y.S. et al. Anti-tumor activity of arginine deiminase via arginine deprivation in retinoblastoma. Oncol. Rep. 2007; 18: 1373–7. DOI: https://doi.org/10.3892/or.18.6.1373
  87. Kim R.H., Coates J.M., Bowles T.L. et al. Arginine deiminase as a novel therapy for prostate cancer induces autophagy and caspase-independent apoptosis. Cancer Res. 2009; 69: 700–8. DOI: https://doi.org/10.1158/0008-5472.CAN-08-3157
  88. Sigimura K., Ohno T., Kusuyama T., Azuma I. High sensitivity of human melanoma cell lines to the growth inhibitory activity of mycoplasmal arginine deiminase in vitro. Melanoma Res. 1992; 2: 191–6. DOI: https://doi.org/10.1097/00008390-199209000-00007
  89. Szlosarek P.W., 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. DOI: https://doi.org/10.1158/1078-0432.CCR-06-1101
  90. Yoon C.Y., Shim Y.J., Kim E.H. et al. Renal cell carcinoma does not express argininosuccinate synthetase and is highly sensitive to arginine deprivation via arginine deiminase. Int. J. Cancer 2008; 120: 897–905. DOI: https://doi.org/10.1002/ijc.22322
  91. Tsai W.B., Aiba I., Lee S.Y. et al. Resistance to arginine deiminase treatment in melanoma cells is associated with induced argininosuccinate synthetase expression involving c-Myc/HIF-1alpha/Sp4. Mol. Cancer Ther. 2009; 8(12): 3223–33. DOI: https://doi.org/10.1158/1535-7163.MCT-09-0794
  92. Ni Y., Liu Y., Schwaneberg U. et al. Rapid evolution of arginine deiminase for improved anti-tumor activity. Appl. Microbiol. Biotechnol. 2011; 90(1): 193–201. DOI: https://doi.org/10.1007/s00253-010-3051-z
  93. Holtsberg F.W., Ensor C.M., Steiner M.R. et al. Poly(ethylene glycol) (PEG) conjugated arginine deiminase: effects of PEG formulations on its pharmacological properties. J. Control. Release 2002; 80: 259–71. DOI: https://doi.org/10.1016/S0168-3659(02)00042-1
  94. Kreis W., Hession C. Biological effects of enzymatic deprivation of Lmethionine in cell culture and an experimental tumor. Cancer Res. 1973; 33(8): 1866–9.
  95. Занин В.А., Лукина В.И., Березов Т.Т. Выделение и некоторые фи- зико-химические и каталитические свойства L-лизин-альфа-оксидазы из Pseudomonas putida. Вопр. мед. хим. 1989; 4: 84–9. [Zanin V.A., Lukina V.I., Berezov T.T. Isolation and some physicochemical and catalytical properties of Pseudomonas putida L-lysine alpha-oxidase. Vopr. med. khim. 1989; 4: 84–9. (In Russ.)].
  96. Манухов И.В., Мамаева Д.В., Морозова Е.А. и др. L-Метионин-гамма- лиаза Citrobacter freundii: клонирование гена и кинетические параметры фермента. Биохим. 2006; 74(4): 454–63. [Manukhov I.V., Mamayeva D.V., Morozova Ye.A. et al. Citrobacter freundii L-methionine gamma-lyase: gene cloning and clinical parameters of enzyme. Biokhim. 2006; 74(4): 454–63. (In Russ.)].
  97. Ito S., Nakamura T., Eguchi Y. Purification and characterization of methioninase from Pseudomonas putida. J. Biochem. 1976; 79(6): 1263–72. DOI: https://doi.org/10.1093/oxfordjournals.jbchem.a131180
  98. Lockwood B.C., Coombs G.H. Purification and characterization of methionine gamma-lyase from Trichomonas vaginalis. Biochem. J. 1991; 279: 675–82. DOI: https://doi.org/10.1042/bj2790675
  99. Sato D., Yamagata W., Kamei K. et al. Expression, purification and crystallization of L-methionine gamma-lyase 2 from Entamoeba histolytica. Acta Crystallogr. 2006; 62(10): 1034–6. DOI: https://doi.org/10.1107/S1744309106036694
  100. Tanaka H., Esaki N., Yamamoto T., Soda K. Purification and properties of methioninase from Pseudomonas ovalis. FEBS Lett. 1976; 66(2): 307–11. DOI: https://doi.org/10.1016/0014-5793(76)80528-5
  101. El-Sayed A.S. Purification and characterization of a new L-methioninase from solid cultures of Aspergillus flavipes. J. Microbiol. 2011; 49(1): 130–40. DOI: https://doi.org/10.1007/s12275-011-0259-2
  102. Пехов А.А., Жукова О.С., Занин В.А., Березов Т.Т. Цитостатический эффект L-метионин-g-лиазы на раковые клетки в культуре. Бюл. эксп. биол. мед. 1983; 5: 87–9. [Pekhov A.A., Zhukova O.S., Zanin V.A., Berezov T.T. Cytostatic effect of L-methionine g-lyase on cultured cancer cells. Byul. eksp. biol. med. 1983; 5: 87–9. (In Russ.)].
  103. Hu J., Cheung N.K. Methionine depletion with recombinant methioninase: in vitro and in vivo efficacy against neuroblastoma and its synergism with chemotherapeutic drugs. Int. J. Cancer 2009; 124(7): 1700–6. DOI: https://doi.org/10.1002/ijc.24104
  104. Kokkinakis D.M., Schold S.C.Jr., Hori H., Nobori T. Effect of long-term depletion of plasma methionine on the growth and survival of human brain tumor xenografts in athymic mice. Nutr. Cancer 1997; 29(3): 195–204. DOI: https://doi.org/10.1080/01635589709514624
  105. Tan Y., Sun X., Xu M. et al. Efficacy of recombinant methioninase in combination with cisplatin on human colon tumors in nude mice. Clin. Cancer Res. 1999; 5(8): 2157–63.
  106. Tan Y., Xu M., Guo H. et al. Anticancer efficacy of methioninase in vivo. Anticancer Res. 1996; 16(6C): 3931–6.
  107. Yoshioka T., Wada T., Uchida N. et al. Anticancer efficacy in vivo and in vitro, synergy with 5-fluorouracil, and safety of recombinant methioninase. Cancer Res. 1998; 58(12): 2583–7.
  108. Hori H., Takabayashi K., Orvis L. et al Gene cloning and characterization of Pseudomonas putida L-methionine-alpha-deamino-gamma-mercaptomethane-lyase. Cancer Res. 1996; 56(9): 2116–22.
  109. El-Sayed A.S., Shouman S.A., Nassrat H.M. Pharmacokinetics, immunogenicity and anticancer efficiency of Aspergillus flavipes L-methioninase. Enzyme Microb. Technol. 2012; 51(4): 200–10. DOI: https://doi.org/10.1016/j.enzmictec.2012.06.004
  110. Tan Y., Zavala J.Sr., Xu M. et al. Serum methionine depletion without side effects by methioninase in metastatic breast cancer patients. Anticancer Res. 1996; 16(6C): 3937–42.
  111. Sun X., Yang Z., Li S. et al. In vivo efficacy of recombinant methioninase is enhanced by the combination of polyethylene glycol conjugation and pyridoxal 5¢-phosphate supplementation. Cancer Res. 2003; 63(23): 8377–83.
  112. Xin L., Cao J., Cheng H. et al. Stealth cationic liposomes modified with anti-CAGE single-chain fragment variable deliver recombinant methioninase for gastric carcinoma therapy. J. Nanosci. Nanotechnol. 2013; 13(1): 178–83. DOI: https://doi.org/10.1166/jnn.2013.6881
  113. Смирнова И.П., Хадуев С.Х. L-лизин-альфа-оксидазная активность некоторых видов Trichoderma. Микробиология 1984; 53: 163–5. [Smirnova I.P., Khaduyev S.Kh. L-lysine alpha-oxidase activity of some Trichoderma spp. Mikrobiologiya 1984; 53: 163–5. (In Russ.)].
  114. Kusakabe H., Kodama K., Kuninaka A. et al. A new antitumor enzyme, L-lysine alpha-oxidase from Trichoderma viride. Purification and enzymological properties. J. Biol. Chem. 1980; 255(3): 976–81. DOI: https://doi.org/10.1016/S0021-9258(19)86128-8
  115. Жукова О.С., Хадуев С.Х., Добрынин Я.В. и др. Влияние L-лизин-a- оксидазы на кинетику клеточного цикла культивируемых клеток лимфомы Беркитта. Экспер. онкол. 1985; 7(6): 42–4. [Zhukova O.S., Khaduyev S.Kh., Dobrynin Ya.V. et al. Influence of L-lysine a-oxidase on kinetics of cell cycle of Burkitt’s lymphoma cultured cells. Eksper. onkol. 1985; 7(6): 42–4. (In Russ.)].
  116. Гогичаева Н.В., Лукашева Е.В., Гаврилова Е.М. и др. Получение конъюгатов L-лизин-a-оксидазы с антителами. Вопр. мед. хим. 2000; 46(4): 410–8. [Gogichayeva N.V., Lukasheva Ye.V., Gavrilova Ye.M. et al. Synthesis of conjugates of L-lysine a-oxidase with antibodies. Vopr. med. khim. 2000; 46(4): 410–8. (In Russ.)].
  117. Лукашева Е.В., Березов Т.Т. L-лизин-a-оксидаза: физико-химиче- ские и биологические свойства. Биохимия 2002; 67(10): 1394–402. [Lukasheva Ye.V., Berezov T.T. L-lysine a-oxidase: physicochemical and biological properties. Biokhimiya 2002; 67(10): 1394–402. (In Russ.)]. DOI: https://doi.org/10.1023/A:1020967408229
  118. Sarkissian C.N., Shao Z., Blain F. et al. A different approach to treatment of phenylketonuria: phenylalanine degradation with recombinant phenylalanine ammonia lyase. Proc. Natl. Acad. Sci. U S A 1999; 96(5): 2339–44. DOI: https://doi.org/10.1073/pnas.96.5.2339
  119. Calabrese J.C., Jordan D.B., Boodhoo A. et al. Crystal structure of phenylalanine ammonia-lyase: multiple helix dipoles implicated in catalysis. Biochemistry 2004; 43: 11403–16. DOI: https://doi.org/10.1021/bi049053+
  120. Ritter H., Schulz G.E. Structural basis for the entrance into the phenylpropanoid metabolism catalyzed by phenylalanine ammonia-lyase. Plant Cell 2004; 16: 3426–36. DOI: https://doi.org/10.1105/tpc.104.025288
  121. Bourget L., Chang T.M. Artificial cell-microencapsulated phenylalanine ammonia-lyase. Applied Biochem. Biotechnol. 1984; 10: 57–9. DOI: https://doi.org/10.1007/978-1-4612-5182-8_5
  122. Sarkissian C.N., Gamez A. Phenylalanine ammonia lyase, enzyme substitution therapy for phenylketonuria, where are we now? Mol. Gen. Metab. 2005; 86(Suppl. 1): S22–6. DOI: https://doi.org/10.1016/j.ymgme.2005.06.016
  123. Abell C.W., Hodgins D.S., Stith W.J. An in vivo evaluation of the chemotherapeutic potency of phenylalanine ammonia-lyase. Cancer Res. 1973; 33(10): 2529–32.
  124. Stith W.J., Hodgins D.S., Abell C.W. Effects of phenylalanine ammonialyase and phenylalanine deprivation on murine leukemic lymphoblasts in vitro. Cancer Res. 1973; 33(5): 966–71.
  125. Ambrus C.M., Anthone S., Horvath C. et al. Extracorporeal enzyme reactors for depletion of phenylalanine in phenylketonuria. Ann. Intern. Med. 1987; 106: 531–7. DOI: https://doi.org/10.7326/0003-4819-106-4-531
  126. Ledoux L. Action of ribonuclease on two solid tumours in vivo. Nature 1955; 176(4470): 36–7. DOI: https://doi.org/10.1038/176036a0
  127. Mitkevich V.A., Tchurikov N.A., Zelenikhin P.V. et al. Binase cleaves cellular noncoding RNAs and affects coding mRNAs. FEBS J. 2010; 277(1): 186–96. DOI: https://doi.org/10.1111/j.1742-4658.2009.07471.x
  128. Darzynkiewicz Z., Carter S.P., Mikulski S.M. et al. Cytostatic and cytotoxic effects of Pannon (P-30 Protein), a novel anticancer agent. Cell Tissue Kinet. 1988; 21(3): 169–82. DOI: https://doi.org/10.1111/j.1365-2184.1988.tb00855.x
  129. Ardelt W., Mikulski S.M., Shogen K. Amino acid sequence of an antitumor protein from Rana pipiens oocytes and early embryos. Homology to pancreatic ribonucleases. Biol. Chem. 1991; 266(1): 245–51. DOI: https://doi.org/10.1016/S0021-9258(18)52427-3
  130. Wu Y., Mikulski S.M., Ardelt W. et al. A cytotoxic ribonuclease. Study of the mechanism of onconase cytotoxicity. J. Biol. Chem. 1993; 268(14): 10686–93. DOI: https://doi.org/10.1016/S0021-9258(18)82252-9
  131. Juan G., Ardelt B., Li X. et al. G1 arrest of U937 cells by onconase is associated with suppression of cyclin D3 expression, induction of p16INK4A, p21WAF1/CIP1 and p27KIP and decreased pRb phosphorylation. Leukemia 1998; 12(8): 1241–8. DOI: https://doi.org/10.1038/sj.leu.2401100
  132. Deptala A., Halicka H.D., Ardelt B. et al. Potentiation of tumor necrosis factor induced apoptosis by onconase. Int. J. Oncol. 1998; 13(1): 11–6. DOI: https://doi.org/10.3892/ijo.13.1.11
  133. Lee I., Kalota A., Gewirtz A.M., Shogen K. Antitumor efficacy of the cytotoxic RNase, ranpirnase, on A549 human lung cancer xenografts of nude mice. Anticancer Res. 2007; 27(1A): 299–307.
  134. Lee I., Lee Y.H., Mikulski S.M., Shogen K. Effect of onconase +/- tamoxifen on ASPC-1 human pancreatic tumors in nude mice. Adv. Exp. Med. Biol. 2003; 530: 187–96. DOI: https://doi.org/10.1007/978-1-4615-0075-9_18
  135. Воробьев И.И., Пономаренко Н.А., Дурова О.М. и др. Структурно- функциональное исследование рекомбинантных форм онконазы. Био- орган. хим. 2001; 27(4): 257–64. [Vorobyev I.I., Ponomarenko N.A., Durova O.M. et al. Structural-functional evaluation of Onconase recombinant forms. Bioorgan. khim. 2001; 27(4): 257–64. (In Russ.)]. DOI: https://doi.org/10.1023/A:1011300402829
  136. Notomista E., Cafaro V., Fusiello R. et al. Effective expression and purification of recombinant onconase, an antitumor protein. FEBS Lett. 1999; 463(3): 211–5. DOI: https://doi.org/10.1016/S0014-5793(99)01623-3
  137. Ita M., Halicka H.D., Tanaka T. et al. Remarkable enhancement of cytotoxicity of onconase and cepharanthine when used in combination on various tumor cell lines. Cancer Biol Ther. 2008; 7(7): 1104–8. DOI: https://doi.org/10.4161/cbt.7.7.6172
  138. Costanzi J., Sidransky D., Navon A. et al. Ribonucleases as a novel pro-apoptotic anticancer strategy: review of the preclinical and clinical data for ranpirnase. Cancer Invest. 2005; 23(7): 643–50. DOI: https://doi.org/10.1080/07357900500283143
  139. Mikulski S.M., Costanzi J.J., Vogelzang N.J. et al. Phase II trial of a single weekly intravenous dose of ranpirnase in patients with unresectable malignant mesothelioma. J. Clin. Oncol. 2002; 20(1): 274–81. DOI: https://doi.org/10.1200/JCO.2002.20.1.274
  140. Porta C., Paglino C., Mutti L. Ranpirnase and its potential for the treatment of unresectable malignant mesothelioma. Biologics 2008; 2(4): 601–9. DOI: https://doi.org/10.2147/BTT.S2383
  141. Chang C.H., Sapra P., Vanama S.S. et al. Effective therapy of human lymphoma xenografts with a novel recombinant ribonuclease/anti-CD74 humanized IgG4 antibody immunotoxin. Blood 2005; 106(13): 4308–14. DOI: https://doi.org/10.1182/blood-2005-03-1033
  142. Calabrese J.C., Jordan D.B., Boodhoo A. et al. Crystal structure of phenylalanine ammonia-lyase: multiple helix dipoles implicated in catalysis. Biochemistry 2004; 43: 11403–16. DOI: https://doi.org/10.1021/bi049053+
  143. Ardelt B., Ardelt W., Pozarowski P. et al. Cytostatic and cytotoxic properties of Amphinase: a novel cytotoxic ribonuclease from Rana pipiens oocytes. Cell Cycle 2007; 24: 3097–102. DOI: https://doi.org/10.4161/cc.6.24.5045
  144. Ильинская О.Н., Зеленихин П.В., Колпаков А.И. и др. Избирательная цитотоксичность биназы в отношении фибробластов, экспрессирующих онкогены ras и AML/ETO. Учен. зап. Казан. ун-та. Серия «Естественные науки» 2008; 150(4): 268–73. [Ilinskaya O.N., Zelenikhin P.V., Kolpakov A.I. et al. Selective binase cytotoxicity against ras- and AML/ETO-oncogene-expressing fibroblasts. Uchen. zap. Kazan. un-ta. Seriya «Estestvennye nauki» 2008; 150(4): 268–73. (In Russ.)].
  145. Mitkevich V.A., Kretova O.V., Petrushanko I.Y. et al. Ribonuclease binase apoptotic signature in leukemic Kasumi-1 cells. Biochemie 2013; 95(6): 1344–9. DOI: https://doi.org/10.1016/j.biochi.2013.02.016
  146. Mitkevich V.A., Petrushanko I.Y., Spirin P.V. et al. Sensitivity of acute myeloid leukemia Kasumi-1 cells to binase toxic action depends on the expression of KIT and АML1-ETO oncogenes. Cell Cycle 2011; 10(23): 4090–7. DOI: https://doi.org/10.4161/cc.10.23.18210

Keywords:

anticancer enzymes, L-asparaginase, -methionine gamma-lyase, L-lysine alpha-oxydase, L-arginine deiminase, L-phenylalanine ammonia-lyase, ranpirnase

License

Copyright (c) 2014 Clinical Oncohematology

Creative Commons License

This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.

Downloads

Download data is not yet available.
2014-1

Downloads

Published

01.01.2014

Issue

Vol. 7 No. 1 (2014)
REVIEWS

How to Cite

Pokrovskiy V.S., Treshchalina H.M. Enzymes in oncohematology: relevant directions of experimental studies and prospects of clinical use. Clinical Oncohematology. Basic Research and Clinical Practice. 2014;7(1):28–38. doi:10.21320/2500-2139-2014-7-1-28-38.