EXPERIMENTAL RESEARCH

Soluble Guanylyl Cyclase (sGC) in Mechanisms of Hypotensive and Antiaggregatory Effects Induced by Teraphtal (TP, sodium salt 4,5-cardoxyphtalocyanin-cobalt)

EXPERIMENTAL RESEARCH , , , , , ,

ТА Sidorova1, NV Pyatakova2, IS Severina2, ОL Kaliya3, GK Gerasimova1

1 N.N. Blokhin Russian Cancer Research Center, 24 Kashirskoye sh., Moscow, Russian Federation, 115478

2 V.N. Orekhovich Institute of Biomedical Chemistry, 10 bld. 8, Pogodinskaya str., Moscow, Russian Federation, 119121

3 State Scientific Center NIOPIC, 1 Bol’shaya Sadovaya str., Moscow, Russian Federation, 123995

For correspondence: Tat’yana Aleksandrovna Sidorova, PhD, 24 Kashirskoye sh., Moscow, Russian Federation, 115478; Tel.: +7(499)612-79-92; e-mail: tatsid@yahoo.com

For citation: Sidorova TA, Pyatakova NV, Severina IS, et al. Soluble Guanylyl Cyclase (sGC) in Mechanisms of Hypotensive and Antiaggregatory Effects Induced by Teraphtal (TP, sodium salt 4,5-cardoxyphtalocyanin-cobalt). Clinical oncohematology. 2016;9(2):138–47 (In Russ).

DOI: 10.21320/2500-2139-2016-9-2-138-147

ABSTRACT

Background & Aims. Many antitumor drugs produces not only the variety of therapeutic effects but also a broad spectrum of side effects, including acute hemodynamic dysfunctions (hypotension/hypertension, coagulation disorders). The aim of the paper is to investigate the role of soluble guanylyl cyclase (sGC) in mechanisms of hypotensive and antiaggregatory effects induced by teraphtal (TP) under experimental conditions in the clinic.

Methods. The effect of different products on the basal activity of sGC isolated from platelets of human peripheral blood was assessed by the immunoenzyme method based on production of cyclic guanosine monophosphate (cGMP). The effect of TP on ADP-induced human platelet aggregation was evaluated by the turbidimetric Born method using an aggregometer.

Results. In the presence of TP, the basal sGC activity increased by the average of 2.5-fold. The TF-induced dose-response curve of sGC activation displays a bell-shaped behavior with maximal stimulation effect achieved at a concentration of 1 mmol/L. TP does not affect the sGC activation induced by known sGC regulators, such as sodium nitroprusside (SNP) and YC-1. On the other hand, after preliminary incubation of sGC with TP, the ability of YC-1 to potentiate the enzyme stimulation induced by SNP decreased by about 33 %. In vitro tests demonstrated the ability of TP to inhibit the ADP-induced platelet aggregation and established the IC50 value for TP (15 mmol/L).

Conclusion. TF is a direct sGC activator and therefore is able to participate in regulation of the NO®sGC®cGMP signaling pathway that controls the basal vascular tone and aggregatory platelet properties. Taking into account the TP characteristics, the paper discusses the involvement of additional mechanisms in the development of hypotension and hemostatic disorders induced by the drug.

Keywords: human platelets, soluble guanylyl cyclase, teraphtal, sodium nitroprusside, YC-1, hypotension, ADP-induced platelet aggregation.

Received: April 24, 2015

Accepted: February 25, 2016

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REFERENCES

  1. Yeh EH, Tong AT, Lenihan DJ, et al. Cardiovascular complications of cancer therapy: diagnosis, pathogenesis, and management. Circulation. 2004;109(25):3122–31. doi: 10.1161/01.cir.0000133187.74800.b9.
  2. Lundin J, Kimby E, Bjorkholm M, et al. Phase II trial of subcutaneous anti-CD52 monoclonal antibody alemtuzumab (Campath-1H) as first-line treatment for patients with B-cell chronic lymphocytic leukemia (B-CLL). Blood. 2002;100(3):768–73. doi: 10.1182/blood-2002-01-0159.
  3. Onrust SV, Lamb HM, Balfour JA. Rituximab. Drugs. 1999;58(1):79–88. doi: 10.2165/00003495-199958010-00009.
  4. Saltz LB, Meropol NJ, Loehrer PJ, et al. Phase II trial of cetuximab in patients with refractory colorectal cancer that expresses the epidermal growth factor receptor. J Clin Oncol. 2004;22(7):1201–8. doi: 10.1200/jco.2004.10.182.
  5. White RL, Schwartzentruber DJ, Guleria A, et al. Cardiopulmonary toxicity of treatment with high dose interleukin-2 in 199 consecutive patients with metastatic melanoma or renal cell carcinoma. Cancer. 1994;74(12):3212–22. doi: 10.1002/1097-0142(19941215)74:12<3212::aid-cncr2820741221>3.0.co;2-i.
  6. Vial T, Descotes J. Immune-mediated side-effects of cytokines in humans. Toxicology. 1995;105(1):31–57. doi: 10.1016/0300-483x(95)03124-x.
  7. Cohen MH, Broder LE, Fossieck BE, et al. Phase II clinical trial of weekly administration of VP-16-213 in small cell bronchogenic carcinoma. Cancer Treat Rep. 1977;61(3):489–90.
  8. Weiss RB, Donehower RC, Wiernik PH, et al. Hypersensitivity reactions from taxol. J Clin Oncol. 1990;8(7):1263–8.
  9. DiBella NJ. Vincristine-induced orthostatic hypotension: a prospective clinical study. Cancer Treat Rep. 1980;64(2–3):359–60.
  10. Zhu GD, Gandhi VB, Gong J, et al. Syntheses of potent, selective, and orally bioavailable indazole-pyridine series of protein kinase B/Akt inhibitors with reduced hypotension. J Med Chem. 2007;50(13):2990–3003. doi: 10.1021/jm0701019.
  11. Orlowski RZ, Stinchcombe TE, Mitchell BS, et al. Phase I trial of the proteasome inhibitor PS-341 in patients with refractory hematologic malignancies. J Clin Oncol. 2002;20(22):4420–7. doi: 10.1200/jco.2002.01.133.
  12. Legha SS, Keating M, Picket S, et al. Phase I clinical investigation of homoharringtonine. Cancer Treat Rep. 1984;68(9):1085–91.
  13. Siderov J, Prasad P, De Boer R, Desai J. Safe administration of etoposide phosphate after hypersensitivity reaction to intravenous etoposide. Br J Cancer. 2002;86(1):12–3. doi: 10.1038/sj.bjc.6600003.
  14. Gelderblom H, Verweij J, Nooter K, Sparreboom A. Cremophor EL: the drawbacks and advantages of vehicle selection for drug formulation. Eur J Cancer. 2001;37(13):1590–8. doi: 10.1016/s0959-8049(01)00171-x.
  15. Itoch Y, Sendo T, Hirakawa T, et al. Role of sensory nerve peptides rather than mast cell histamine in paclitaxel hypersensitivity. Am J Respir Crit Care Med. 2004;169(1):113–9. doi: 10.1164/rccm.200307-901oc.
  16. Carmichael SM, Eagleton L, Ayers CR. Orthostatic hypotension during vincristine therapy. Arch Intern Med. 1970;126(2):290–3. doi: 10.1001/archinte.1970.00310080096015.
  17. Renninger JP, Murphy DJ, Morel DW. A selective Akt inhibitor produces hypotension and bradycardia in conscious rats due to inhibition of the autonomic nervous system. Toxicol Sci. 2012;125(2):578–85. doi: 10.1093/toxsci/kfr316.
  18. Akosman C, Ordu C, Eroglu E, Oyan B. Development of Acute Pulmonary Hypertension After Bortezomib Treatment in a Patient With Multiple Myeloma: A Case Report and the Review of the Literature. Am J Ther. 2013;22(3):e88–92. doi: 10.1097/01.mjt.0000433941.91996.5f.
  19. Richardson PG, Mitsiades C, Hideschima T, Anderson KC. Bortezomib: proteosome inhibition as an effective anticancer therapy. Annu Rev Med. 2006;57(1):33–47. doi: 10.1146/annurev.med.57.042905.122625.
  20. Savaraj N, Lu K, Feun LG, et al. Interaction of [3H] homoharringtonine (HHT) with the calcium antagonist receptor in the rat. Proc Am Assoc Cancer Res. 1985;26:1417.
  21. Yang ZZ, Tschopp O, Baudry A, et al. Physiological functions of protein kinase B/Akt. Biochem Soc Trans. 2004;32(Pt 2):350–4. doi: 10.1042/bst0320350.
  22. Yeh ET. Cardiotoxicity induced by chemotherapy and antibody therapy. Annu Rev Med. 2006;57(1):485–98. doi: 10.1146/annurev.med.57.121304.131240.
  23. Senkus E, Jassem J. Cardiovascular effects of systemic cancer treatment. Cancer Treat Rev. 2011;37(4):300–11. doi: 10.1016/j.ctrv.2010.11.001.
  24. Yang JC, Haworth L, Sherry RM, et al. A randomized trial of bevacizumab, an anti-vascular endothelial growth factor antibody, for metastatic renal cancer. N Engl J Med. 2003;349(5):427–34. doi: 10.1056/nejmoa021491.
  25. Gordon MS, Margolin K, Talpaz M, et al. Phase I safety and pharmacokinetic study of recombinant human anti-vascular endothelial growth factor in patients with advanced cancer. J Clin Oncol. 2001;19(3):843–50.
  26. Motzer RJ, Hutson TE, Tomczak P, et al. Sunitinib versus interferon alfa in metastatic renal-cell carcinoma. N Engl J Med. 2007;356(2):115–24. doi: 10.1056/nejmoa065044.
  27. Gupta R, Maitland ML. Sunitinib, Hypertension, and Heart Failure: A Model for Kinase Inhibitor-Mediated Cardiotoxicity. Curr Hypertens Rep. 2011;13(6):430–5. doi: 10.1007/s11906-011-0229-4..
  28. Rini BI, Cohen DP, Lu DR, et al. Hypertension as a biomarker of efficacy in patients with metastatic renal cell carcinoma treated with sunitinib. J Natl Cancer Inst. 2011;103(9):763–73. doi: 10.1093/jnci/djr128.
  29. Mourad JJ, Levy BI. Mechanisms of antiangiogenic-induced arterial hypertension. Curr Hypertens Rep. 2011;13(4):289–93. doi: 10.1007/s11906-011-0206-y.
  30. Kamba T, McDonald DM. Mechanisms of adverse effects of anti-VEGF therapy for cancer. Br J Cancer. 2007;96(12):1788–95. doi: 10.1038/sj.bjc.6603813.
  31. Aparicio-Gallego G, Afonso-Afonso FJ, Leon-Mateos L, et al. Molecular basis of hypertension side effects induced by sunitinib. Anticancer Drugs. 2011;22(1):1–8. doi: 10.1097/CAD.0b013e3283403806.
  32. Facemire CS, Nixon AB, Griffiths R, et al. Vascular endothelial growth factor receptor 2 controls blood pressure by regulating nitric oxide synthase expression. Hypertension. 2009;54(3):652–8. doi: 10.1161/HYPERTENSIONAHA.109.129973.
  33. Olsson AK, Dimberg A, Kreuger J, Claesson-Welsh L. VEGF receptor signalling – in control of vascular function. Nat Rev Mol Cell Biol. 2006;7(5):359–71. doi: 10.1038/nrm1911.
  34. Ignarro LJ. Nitric oxide: a unique endogenous signaling molecule in vascular biology. Biosci Rep. 1999;19:51–71.
  35. Denninger JW, Marletta MA. Guanylate cyclase and the NO/cGMP signaling pathway. Biochim Biophys Acta. 1999;1411(2–3):334–50. doi: 10.1016/s0005-2728(99)00024-9.
  36. Daher IN, Yeh ET. Vascular complications of selected cancer therapies. Nat Clin Pract Cardiovasc Med. 2008;5(12):797–805. doi: 10.1038/ncpcardio1375.
  37. Aharon IB, Joseph HB, Tzabari M, et al. Doxorubicin-induced vascular toxicity –targeting potential pathways may reduce procoagulant activity. PLoS One. 2013;8(9):e75157. doi: 10.1371/journal.pone.0075157.
  38. Togna GI, Togna AR, Franconi M, Caprino L. Cisplatin Triggers Platelet Activation. Thromb Res. 2000;99(5):503–9. doi: 10.1016/s0049-3848(00)00294-2.
  39. Yeh ET, Bickford CL. Cardiovascular complications of cancer therapy: incidence, pathogenesis, diagnosis, and management. J Am Coll Cardiol. 2009;53(24):2231–47. doi: 10.1016/j.jacc.2009.02.050.
  40. Martin JF, Greaves M. Vincristine inhibits the synthesis of malondialdehyde by human platelets in vitro. Cancer. 1982;49(4):665–8. doi: 10.1002/1097-0142(19820215)49:4<665::aid-cncr2820490413>3.0.co;2-y.
  41. Lee JJ, Yu JY, Lee JH, et al. The protective effects of paclitaxel on platelet aggregation through the inhibition of thromboxane A2 synthase. Arch Pharm Res. 2010;33(3):387–94. doi: 10.1007/s12272-010-0307-1.
  42. Ермакова Н.П., Михайлова Л.М., Трифонов А.И. и др. Влияние терафтала и бинарной каталитической системы «Терафтал+аскорбиновая кислота» на артериальное давление. Российский биотерапевтический журнал. 2006;5(1):14.
    [Ermakova NP, Mikhailova LM, Trifonov AI, et al. Effect of teraphtal and binary catalytic system “Teraphtal+ascorbic acid” on blood pressure. Rossiiskii bioterapevticheskii zhurnal. 2006;5(1):14. (In Russ)]
  43. Маджуга А.В., Ермакова Н.П., Членова Е.Л. и др. Влияние терафтала-лио на гемостаз животных. Вопросы онкологии. 2001;47(6):715–7.
    [Madzhuga AV, Ermakova NP, Chlenova EL, et al. Effect of teraphtal-lio on animals’ hemostasis. Voprosy onkologii. 2001;47(6):715–7. (In Russ)]
  44. Манзюк Л.В., Бредер В.В., Гершанович М.Л. и др. Результаты I-II фазы клинических испытаний каталитической системы «Терафтал+аскорбиновая кислота». Российский биотерапевтический журнал 2005;4(1):105–7.
    [Manzyuk LV, Breder VV, Gershanovich ML, et al. Results of Phase I-II clinical trials of catalytic system “Teraphtal+ascorbic acid”. Rossiiskii bioterapevticheskii zhurnal. 2005;4(1):105–7. (In Russ)]
  45. Mingone CJ, Gupte SA, Chow JL, et al. Protoporphyrin IX generation from delta-aminolevulinic acid elicits pulmonary artery relaxation and soluble guanylate cyclase activation. Am J Physiol Lung Cell Mol Physiol. 2006;291(3):L337–44. doi: 10.1152/ajplung.00482.2005.
  46. Sharina I, Sobolevsky M, Doursout MF, et al. Coinamides are novel coactivators of oxide receptor that target soluble guanylyl cyclase catalytic domain. J Pharmacol Exp Ther 2012;340(3):723–32. doi: 10.1124/jpet.111.186957.
  47. Martin E, Sharina I, Liang YY, Doursout MF. Corrin-mediated activation of nitric oxide receptor and its cardiovascular consequences. Circulation. 2009;120:S1072. Abstract 5218.
  48. Чирков Ю.Ю., Тыщук И.А., Белушкина Н.Н., Северина И.С. Гуанилатциклаза тромбоцитов крови человека. Биохимия. 1987;52(6):956–63.
    [Chirkov YuYu, Tyshchuk IA, Belushkina NN, Severina IS. Guanylyl cyclase of human platelets. Biokhimiya. 1987;52(6):956–63. (In Russ)]
  49. Garbers DL, Murad F. Guanylate cyclase assay methods. Adv Cyclic Nucleotide Res. 1979;10:57–67.
  50. Born GVR. Aggregation of blood platelets by adenosine diphosphate and its reversal. Nature. 1962;194(4832):927–9. doi: 10.1038/194927b0.
  51. Bellamy TC, Garthwaite J. The receptor-like properties of nitric oxide-activated soluble guanylyl cyclase in intact cells. Mol Cell Biochem. 2002;230(1–2):165–76.
  52. Gibb B, Wykes V, Garthwaite J. Properties of NO-activaed guanylyl cyclases expressed in cells. Br J Pharmacol. 2003;139(5):1032–40. doi: 10.1038/sj.bjp.0705318.
  53. Proinsias K, Gryko DT, Hisaeda Y, et al. Vitamin B12 derivatives as activators of soluble guanylyl cyclase. J Med Chem. 2012;55(20):8943–7. doi: 10.1021/jm3006959.
  54. Bindslev N. A homotropic two-state model and auto-antagonism. BMC Pharmacol. 2004;4(1):11. doi: 10.1186/1471-2210-4-11.
  55. Ignarro LJ, Wood KS, Wolin MS. Activation of purified soluble guanylate cyclase by protoporphyrin IX. Proc Natl Acad Sci USA. 1982;9:2870–3. doi: 10.1073/pnas.79.9.2870.
  56. Ko FN, Wu CC, Kuo SC, et al. YC-1, a novel activator of platelet guanylate cyclase. Blood. 1994;84(12):4226–33.
  57. Chun YS, Yeo EJ, Park JW. Versatile pharmacological actions of YC-1: anti-platelet to anticancer. Cancer Lett. 2004;207(1):1–7. doi: 10.1016/j.canlet.2004.01.005.
  58. Rapoport RM, Murad F. Agonist-induced endothelium-dependent relaxation in rat thoracic aorta may be mediated through cGMP. Circ Res. 1983;52(3):352–7. doi: 10.1161/01.res.52.3.352.
  59. Herman MA, Webber J, Fromm D, Kessel D. Hemodynamic effects of 5-aminolevulinic acid in humans. J Photochem Photobiol B. 1998;43(1):61–5. doi: 10.1016/s1011-1344(98)00086-4.
  60. Chung IW, Eljamel S. Risk factors for developing oral 5-aminolevulinic acid-induced side effects in patients undergoing fluorescence guided resection. Photodiagn Photodyn Ther. 2013;10(4):362–7. doi: 10.1016/j.pdpdt.2013.03.007.
  61. Rothermund L, Friebe A, Paul M, et al. Acute blood pressure effects of YC-1-induced activation of soluble guanylyl cyclase in normotensive and hypertensive rats. Br J Pharmacol. 2000;130(2):205–8. doi: 10.1038/sj.bjp.0703320.
  62. Friebe A, Mullershausen F, Smolenski A, et al. YC-1 potentiates nitric oxide- and carbon monoxide-induced cyclic GMP effects in human platelets. Mol Pharmacol. 1998;54(6):962–7.
  63. Severina IS. Nitric oxide. Potentiation of NO-dependent activation of soluble guanylate cyclase – (patho)physiological and pharmacotherapeutical significance. Biomed Khim. 2007;53(4):385–99.
  64. Герасимова Г.К., Якубовская Р.И., Панкратов А.А. и др. Бинарная каталитическая терапия — новый подход к лечению злокачественных опухолей. Результаты доклинических и клинических исследований. Российский химический журнал. 2013;LVII(2):69–82.
    [Gerasimova GK, Yakubovskaya RI, Pankratov AA, et al. Binary catalytic therapy: new approach to treatment of malignancies. Results of pre-clinical and clinical studies. Rossiiskii khimicheskii zhurnal. 2013;LVII(2):69–82. (In Russ)]
  65. Broderick KE, Singh V, Zhuang S, et al. Nitric oxide scavenging by the cobalamin precursor cobinamide. J Biol Chem. 2005;280(10):8678–85. doi: 10.1074/jbc.m410498200.
  66. Ignarro LJ. Experimental evidences of nitric oxide-dependent vasodilatory activity of nebivolol, a third-generation beta-blocker. Blood Press. 2004;13(Suppl 1):2–16. doi: 10.1080/08038020410016557.
  67. Герасимова Г.К., Сидорова Т.А., Солнцева Т.И. и др. Бинарная каталитическая терапия — новый подход к контролю роста опухолевых клеток с помощью высокореактивных радикалов кислорода. Российский биотерапевтический журнал. 2006;5(3):98–105.
    [Gerasimova GK, Sidorova TA, Solntseva TI, et al. Binary catalytic therapy – a new approach to control of malignant tumors growth by reactive oxygen species. Rossiiskii bioterapevticheskii zhurnal. 2006;5(3):98–105. (In Russ)]
  68. Rosendorff C. Beta-blocking agents with vasodilator activity (Short Survey). J Hypertens. 1993;11(Suppl 4):S37–40. doi: 10.1097/00004872-199306003-00009.
  69. Seitz S, Wegener JW, Rupp J, et al. Involvement of K(+) channels in the relaxant effects of YC-1 in vascular smooth muscle. Eur J Pharmacol. 1999;382(1):11–8. doi: 10.1016/s0014-2999(99)00574-9.
  70. Boerrigter G, Burnett JC Jr. Nitric oxide-independent stimulation of soluble guanylate cyclase with BAY 41-2272 in cardiovascular disease. Cardiovasc Drug Rev. 2007;25(1):30–45. doi: 10.1111/j.1527-3466.2007.00003.x.
  71. Hardman JG, Davis JW, Sutherland EW. Effects of some hormonal and other factors on the excretion of guanosine 3¢,5¢-monophosphate and adenosine 3¢,5¢-monophosphate in rat urine. J Biol Chem. 1969;244(23):6354–62.
  72. Silva BR, Pernomian L, Grando MD, Bendhack LM. Phenylephrine activates eNOS Ser 1177 phosphorylation and nitric oxide signaling in renal hypertensive rat aorta. Eur J Pharmacol. 2014;738:192–9. doi: 10.1016/j.ejphar.2014.05.040.
  73. Hilgers RHP, Oparil S, Wouters W, Coelingh Bennink HJT. Vasorelaxing effects of estetrol in rat arteries. J Endocrinol. 2012;215(1):97–106. doi: 10.1530/JOE-12-0009.
  74. Nossaman B, Pankey E, Kadowitz P. Stimulators and activators of soluble guanylate cyclase: review and potential therapeutic indications. Crit Care Res Pract. 2012;2012:290805. doi: 10.1155/2012/290805.
  75. Mellion BT, Ignarro LJ, Ohlstein EH, et al. Evidence for the inhibitory role of guanosine 3¢,5¢-monophosphate in ADP-induced human platelet aggregation in the presence of nitric oxide and related vasodilators. Blood. 1981;57(5):946–55.
  76. Gachet C. P2 receptors, platelet function and pharmacological implications. Thromb Haemost. 2008;99(3):466–72. doi: 10.1160/TH07-11-0673.
  77. Roger S, Badier-Commander C, Paysant J, et al. The anti-aggregating effect of BAY 41-2272, a stimulator of soluble guanylyl cyclase, requires the presence of nitric oxide. Br J Pharmacol. 2010;161(5):1044–58. doi: 10.1111/j.1476-5381.2010.00943.x.

Ribonucleases with Antiproliferative Properties: Molecular Biological and Biochemical Characteristics

EXPERIMENTAL RESEARCH , , , , ,

VS Pokrovskii1, EM Treshchalina1, NV Andronova1, SM Deev2

1 N.N. Blokhin Russian Cancer Research Center, 24 Kashirskoye sh., Moscow, Russian Federation, 115478

2 M.M. Shemyakin and Yu.A. Ovchinnikov Institute of Bioorganic Chemistry, 16/10 Miklukho-Maklaya str., Moscow, Russian Federation, 117997

For correspondence: Vadim Sergeevich Pokrovskii, PhD, 24 Kashirskoye sh., Moscow, Russian Federation, 115478; Tel.: +7(499)324-14-09; e-mail: vadimpokrovsky@yandex.ru

For citation: Pokrovskii VS, Treshchalina EM, Andronova NV, Deev SM. Ribonucleases with Antiproliferative Properties: Molecular Biological and Biochemical Characteristics. Clinical oncohematology. 2016;9(2):130–7 (In Russ).

DOI: 10.21320/2500-2139-2016-9-2-130-137

ABSTRACT

The article dwells on ribonucleases (RNAses) whose cytotoxic activity depends on the enzymatic activity, i.e. the ability to catalyze the cleavage of phosphodiester bonds of RNA. It presents both well-known information and our own data on RNAses of different origins with antitumor properties; it investigates the relation between the mechanism of cytotoxicity and biochemical and molecular biological characteristics. The analysis of published data demonstrates that all above characteristics contribute to the antiproliferative activity of RNAses. The major challenge for this group of enzymes is the achieving of selective bioavailability. This problem can be solved by creating conjugates as in case with ranpirnase and barnase. Based on their major pharmacological properties, active antitumor RNAses have great perspectives for treatment of not only oncohematological, but also solid malignancies.

Keywords: ribonucleases, ranpirnase, amphinase, binase, barnase, pharmacological properties.

Received: January 4, 2016

Accepted: January 7, 2016

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REFERENCES

  1. Deutscher MP, Li Z. Exoribonucleases and their multiple roles in RNA metabolism. Prog Nucl Acid Res Mol Biol. 2001;66:67–105. doi: 10.1016/s0079-6603(00)66027-0.
  2. Зеленихин П.В., Мамедзаде К.Р., Ильинская О.Н. Цитофлуориметрическая характеристика влияния РНКаз на клетки про- и эукариот. Гены и клетки. 2012;3(7):62–5.
    [Zelenikhin PV, Mamedzade KR, Ilinskaya ON. The cytofluorimetric characteristics of RNAse influence towards pro- and eucariotic cells. Geny i kletki. 2012;3(7):62–5. (In Russ)]
  3. Ledoux L. Action of ribonuclease on two solid tumours in vivo. Nature. 1955;176(4470):36–7. doi: 10.1038/176036a0.
  4. Edelweiss E, Balandin TG, Ivanova JL, et al. Barnase as a new therapeutic agent triggering apoptosis in human cancer cells. PLoS ONE. 2008;3(6):e2434. doi: 10.1371/journal.pone.0002434.
  5. Глинка Е.М., Эдельвейс Э.Ф., Деев С.М. Эукариотические экспрессирующие векторы и иммуноконъюгаты для терапии рака. Биохимия. 2006;71:597–60.
    [Glinka EM, Edel’veis EF, Deev SM. Eukaryotic expressing vectors and immunoconjugates for treatment of cancer. Biokhimiya. 2006;71:597–60. (In Russ)]
  6. Deyev SM, Lebedenko EN, Petrovskaya LE, et al. Man-made antibodies and immunoconjugates with desired properties: function optimization using structure engineering. Russ Chem Rev. 2015;84(1):1–26. doi: 10.1070/RCR4459.
  7. Mitkevich VA, Tchurikov NA, Zelenikhin PV, et al. Binase cleaves cellular noncoding RNAs and affects coding mRNAs. FEBS J. 2010;277(1):186–96. doi: 10.1111/j.1742-4658.2009.07471.x.
  8. Кабрера Фуентес Э.А., Зеленихин П.В., Колпаков А.И. и др. Сравнительная цитотоксичность биназы по отношению к опухолевым и нормальным клеткам. Ученые записки Казанского университета. Серия: Естественные науки. 2010;152(3):143–8.
    [Caberra Fuentes HA, Zelenikhin PV, Kolpakov AI, et al. Comparative Toxicity of Binase towards Tumor and Normal Cells. Uchenye zapiski Kazanskogo universiteta. Seriya: Estestvennye nauki. 2010;152(3):143–8. (In Russ)]
  9. Darzynkiewicz Z, Carter SP, Mikulski SM, et al. Cytostatic and cytotoxic effects of Pannon (P-30 Protein), a novel anticancer agent. Cell Tissue Kinet. 1988;21(3):169–82. doi: 10.1111/j.1365-2184.1988.tb00855.x.
  10. Ardelt W, Mikulski SM, Shogen K. Amino acid sequence of an anti-tumor protein from Rana pipiens oocytes and early embryos. Homology to pancreatic ribonucleases. Biol Chem. 1991;266(1):245–51.
  11. Raines RT. Active site of ribonuclease A. In: Zenkova MA, ed. Artificial Nucleases. Heidelberg: Springer Verlag; 2004. pp. 19–32.
  12. Juan G, Ardelt B, Mikulski SM, et al. G1 arrest of U-937 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: 10.1038/sj.leu.2401100.
  13. Deptala A, Halicka HD, Ardelt B, et al. Potentiation of tumor necrosis factor induced apoptosis by onconase. Int J Oncol. 1998;13(1):11–6. doi: 10.3892/ijo.13.1.11.
  14. Tsai SY, Ardelt B, Hsieh TC, et al. Treatment of Jurkat acute T-lymphocytic leukemia cells by onconase (Ranpirnase) is accompanied by an altered nucleocytoplasmic distribution and reduced expression of transcription factor NF-kappaB. Int J Oncol. 2004;25(6):1745–52. doi: 10.3892/ijo.25.6.1745.
  15. Rodriguez M, Torrent G, Bosch M, et al. Intracellular pathway of Onconase that enables its delivery to the cytosol. J Cell Sci. 2007;120(8):1405–11. doi: 10.1242/jcs.03427.
  16. Marquez M, Nilsson S, Lennartsson L, et al. Charge dependent targeting: Results in six tumor cell lines. Anticancer Res. 2004;24:1347–51.
  17. Leland PA, Raines RT. Cancer chemotherapy: ribonucleases to the rescue. Chem Biol. 2001;8(5):405–13. doi: 10.1016/s1074-5521(01)00030-8.
  18. Wu Y, Mikulski SM, Ardelt W, et al. A cytotoxic ribonuclease. Study of the mechanism of onconase cytotoxicity. J Biol Chem. 1993;268(14):10686–93.
  19. Saxena SK, Sirdeshmukh R, Ardelt W, et al. Entry into cells and selective degradation of tRNAs by a cytotoxic member of the RNase A family. J Biol Chem. 2002;277(17):15142–6. doi: 10.1074/jbc.m10811520020.
  20. Suhasini AN, Sirdeshmukh R. Transfer RNA cleavages by onconase reveal unusual cleavage sites. J Biol Chem. 2006;281(18):12201–9. doi: 10.1074/jbc.m504488200.
  21. Gong J, Li X, Darzynkiewicz Z. Different patterns of apoptosis of HL-60 cells induced by cycloheximide and camptothecin. J Cell Physiol. 1993;157(2):263–70. doi: 10.1002/jcp.1041570208.
  22. Ardelt B, Ardelt W, Darzynkiewicz Z. Cytotoxic ribonucleases and RNA interference (RNAi). Cell Cycle 2003;2(1):22–4. doi: 10.4161/cc.2.1.232.
  23. Zhao H, Ardelt B, Ardelt W, et al. The cytotoxic ribonuclease Onconase targets RNA interference (siRNA). Cell Cycle. 2008;7(20):3258–61. doi: 10.4161/cc.7.20.6855.
  24. Volinia S, Calin GA, Liu CG, et al. A microRNAs expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA. 2006;103(7):2257–61. doi: 10.1073/pnas.0510565103.
  25. Basseres DS, Baldwin AS. Nuclear factor-kappaB and inhibitor of kappaB kinase pathways in oncogenic initiation and progression. Oncogene. 2006;30(25):6817–30. doi: 10.1038/sj.onc.1209942.
  26. Lee I, Kalota A, Gewirtz AM, 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.
  27. Lee I, Lee YH, Mikulski SM, Shogen K. Effect of onconase +/- tamoxifen on ASPC-1 human pancreatic tumors in nude mice. Adv Exp Med Biol. 2003;530:187–96. doi: 10.1007/978-1-4615-0075-9_18
  28. Rybak SM, Pearson JW, Fogler WE, et al. Enhancement of vincristine cytotoxicity in drug-resistant cells by simultaneous treatment with onconase, an antitumor ribonuclease. J Natl Cancer Inst. 1996;88(11):747–53. doi: 10.1093/jnci/88.11.747.
  29. Ita M, Halicka HD, 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: 10.4161/cbt.7.7.6172.
  30. Smolewski P, Witkowska M, Zwolinska M, et al. Cytotoxic activity of the amphibian ribonucleases onconase and r-amphinase on tumor cells from B cell lymphoproliferative disorders. Int J Oncol. 2014;45(1):419–25. doi: 10.3892/ijo.2014.2405.
  31. Majchrzak A, Witkowska M, Medra A, et al. In vitro cytotoxicity of ranpirnase (onconase) in combination with components of R-CHOP regimen against diffuse large B cell lymphoma (DLBCL) cell line. Postepy Hig Med Dosw. 2013;67:1166–72. doi: 10.5604/17322693.107838632.
  32. Porta C, Paglino C, Mutti L. Ranpirnase and its potential for the treatment of unresectable malignant mesothelioma. Biologics. 2008;2(4):601–9. doi: 10.2147/btt.s2383.
  33. 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: 10.1080/07357900500283143.
  34. Mikulski SM, Costanzi JJ, Vogelzang NJ, 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: 10.1200/jco.20.1.274.
  35. Vasandani VM, Burris JA, Sung C. Reversible nephrotoxicity of onconase and effect of lysine pH on renal onconase uptake. Cancer Chemother Pharmacol. 1999;44(2):164–9. doi: 10.1007/s002800050962.
  36. Singh UP, Ardelt W, Saxena SK, et al. Enzymatic and Structural Characterisation of Amphinase, a Novel Cytotoxic Ribonuclease from Rana pipiens Oocytes. J Mol Biol. 2007;371(1):93–111. doi: 10.1016/j.jmb.2007.04.071.
  37. 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;6(24):3097–102. doi: 10.4161/cc.6.24.5045.
  38. Sevcik J, Sanishili RG, Pavlovsky AG, Polyakov KM. Comparison of active sites of some microbial ribonucleases: structural basis for guanylic specificity. Trends Biochem Sci. 1990;15(4):158–62. doi: 10.1016/0968-0004(90)90217-y.
  39. Makarov AA, Ilinskaya ON. Cytotoxic ribonucleases: molecular weapons and their targets. FEBS Lett. 2003;540(1–3):15–20. doi: 10.1016/s0014-5793(03)00225-4.
  40. Makarov AA, Kolchinski A, Ilinskaya ON. Binase and other microbial RNases as potential anticancer agents. BioEssays. 2008;30(8):789–90. doi: 10.1002/bies.20789.
  41. Ильинская О.Н., Макаров А.А. Почему рибонуклеазы вызывают гибель раковых клеток. Молекулярная биология. 2005;39(1):3–13.
    [Il’inskaya ON, Makarov AA. Why ribonucleases cause tumor cell death. Molekulyarnaya biologiya. 2005;39(1):3–13. (In Russ)]
  42. Ильинская О.Н., Зеленихин П.В., Колпаков А.И. и др. Избирательная цитотоксичность биназы в отношении фибробластов, экспрессирующих онкогены ras и AML/ETO. Ученые записки Казанского университета. Серия: Естественные науки. 2008;150(4):268–73.
    [Ilinskaya ON, Zelenikhin PV, Kolpakov AI, et al. Selective Cytotoxicity of Binase towards Fibroblasts with Expression of the ras- and AML/ETO Oncogenes. Uchenye zapiski Kazanskogo universiteta. Seriya: Estestvennye nauki. 2008;150(4):268–73. (In Russ)]
  43. Mitkevich VA, Petrushanko IY, Spirin PV, 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: 10.4161/cc.10.23.18210.
  44. Mitkevich VA, Kretova OV, Petrushanko IY, et al. Ribonuclease binase apoptotic signature in leukemic Kasumi-1 cells. Biochimie. 2013;95(6):1344–9. doi: 10.1016/j.biochi.2013.02.016.
  45. Петрушанко И.Ю., Зеленихин П.В., Митькевич В.А. и др. Биназа обладает избирательным цитотоксическим действием на kit-трансформированные предшественники миелоидных клеток. Биофизика. 2007;52(5):876–81.
    [Petrushanko IYu, Zelenikhin PV, Mit’kevich VA, et al. Binasa produces selective cytotoxic effect on kit-transformed myeloid cell precursors. Biofizika. 2007;52(5):876–81. (In Russ)]
  46. Зеленихин П.В., Колпаков А.И., Черепнев Г.В., Ильинская О.Н. Индукция апоптоза опухолевых клеток биназой. Молекулярная биология. 2005;39(3):457–63.
    [Zelenikhin PV, Kolpakov AI, Cherepnev GV, Il’inskaya ON. Induction of tumor cell apoptosis by binasa. Molekulyarnaya biologiya. 2005;39(3):457–63. (In Russ)]
  47. Трещалина Е.М. Коллекция опухолевых штаммов человека. М.: Практическая медицина, 2009. 70 с.
    [Treshchalina EM. Kollektsiya opukholevykh shtammov cheloveka. (Collection of human tumor strains.) Moscow: Prakticheskaya Meditsina Publ.; 2009. 70 p. (In Russ)]
  48. Трещалина Е.М. Иммунодефицитные мыши разведения РОНЦ им. Н.Н. Блохина РАМН. Возможности использования. М.: Издательская группа РОНЦ, 2010. 16 с.
    [Treshchalina EM. Immunodefitsitnye myshi razvedeniya RONTs im. N.N. Blokhina RAMN. Vozmozhnosti ispol’zovaniya. (Mice with immune deficiency bred in NN Blokhin Russian Cancer Research Center. Opportunities for use.) Moscow: Izdatel’skaya gruppa RONTs Publ.; 2010. 16 p. (In Russ)]
  49. Трещалина Е.М., Жукова О.С., Герасимова Г.К. и др. Методические рекомендации по доклиническому изучению противоопухолевой активности лекарственных средств. В кн.: Руководство по проведению доклинических исследований лекарственных средств. Часть первая. М.: Гриф и К, 2012. С. 642–57.
    [Treshchalina EM, Zhukova OS, Gerasimova GK, et al. Guidelines for pre-clinical studies of antitumor activity of drugs. In: Rukovodstvo po provedeniyu doklinicheskikh issledovanii lekarstvennykh sredstv. (Guidelines for pre-clinical studies of medicinal agents.) Part 1. Moscow: Grif i K Publ.; 2012. pp. 642–57. (In Russ)]
  50. Ulyanova V, Vershinina V, Ilinskaya O. Barnase and binase: twins with distinct fates. FEBS J. 2011;8(19):3633–43. doi: 10.1111/j.1742-4658.2011.08294.x.
  51. Hoefling M, Gottschalk KE. Barnase–barstar: from first encounter to final complex. J Struct Biol. 2010;171(1):52–63. doi: 10.1016/j.jsb.2010.03.001.
  52. Deyev SM, Yazynin SA, Kuznetsov DA, et al. Ribonuclease-charged vector for facile direct cloning with positive selection. Mol Gen Genet. 1998;259(4):379–82. doi: 10.1007/s004380050825.
  53. Semenyuk EG, Stremovskiy OA, Edelweiss EF, et al. Expression of single-chain antibody–barstar fusion in plants. Biochimie. 2007;89(1):31–8. doi: 10.1016/j.biochi.2006.07.012.
  54. Liao YD, Huang HC, Chan HJ, Kuo SJ. Large-scale preparation of a ribonuclease from Rana catesbeiana (bullfrog) oocytes and characterization of its specific cytotoxic activity against tumor cells. Prot Express Purif. 1996;7(2):194–202. doi: 10.1006/prep.1996.0027.
  55. Tatsuta T, Sugawara S, Takahashi K, et al. Cancer-selective induction of apoptosis by leczyme. Front Oncol. 2014;4:139. doi: 10.3389/fonc.2014.00139.
  56. Zhang R, Zhao L, Wang H, Ng TB. A novel ribonuclease with antiproliferative activity toward leukemia and lymphoma cells and HIV-1 reverse transcriptase inhibitory activity from the mushroom, Hohenbuehelia serotina. Int J Mol Med. 2014;33(1):209–14.
  57. Tatsuta T, Sugawara S, Takahashi K, et al. Leczyme: A New Candidate Drug for Cancer Therapy. BioMed Re Intern. 2014. doi: 10.1155/2014/421415.
  58. Nitta K, Ozaki K, Ishikawa M, et al. Inhibition of cell proliferation by Rana catesbeiana and Rana japonica lectins belonging to the ribonuclease superfamily. Cancer Res. 1994;54(4):920–7.
  59. Tatsuta T, Hosono M, Sugawara S, et al. Sialic acid-binding lectin (leczyme) induces caspase-dependent apoptosis-mediated mitochondrial perturbation in Jurkat cells. Intern J Oncol. 2013;43(5):1402–12. doi: 10.3892/ijo.2013.2092.
  60. Glinka EM, Edelweiss EF, Sapozhnikov AM, Deyev SM. A new vector for controllable expression of an anti-HER2/neu mini-antibody-barnase fusion protein in HEK 293T cells. Gene. 2006;366(1):97–103. doi: 10.1016/j.gene.2005.06.042.
  61. Chang CH, Sapra P, Vanama SS, 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: 10.1182/blood-2005-03-1033.
  62. Newton DL, Stockwin LH, Rybak SM. Anti-CD22 Onconase: preparation and characterization. Meth Mol Biol. 2009;525:425–43. doi: 10.1007/978-1-59745-554-1_22.
  63. Newton DL, Hansen HJ, Mikulski SM, et al. Potent and specific antitumor effects of an anti-CD22-targeted cytotoxic ribonuclease: potential for the treatment of non-Hodgkin lymphoma. Blood. 2001;97(2):528–35. doi: 10.1182/blood.v97.2.528.
  64. Глинка Е.M., Эдельвейс Э.Ф., Деев С.М. Эукариотические экспрессирующие векторы и иммуноконъюгаты для терапии рака. Биохимия. 2006;71(6):742–53.
    [Glinka EM, Edel’veis EF, Deev SM. Eukaryotic expressing vectors and immunoconjugates for treatment of cancer. Biokhimiya. 2006;71(6):742–53. (In Russ)]
  65. Deyev SM, Lebedenko EN. Modern technologies for creating synthetic antibodies for clinical application. Acta Naturae. 2009;1(1):32–50.
  66. Эдельвейс Э.Ф. Иммунобарназные конъюгаты для диагностики и терапии рака: Автореф. дис. ¼ канд. биол. наук. М., 2010. 24 с.
    [Edel’veis EF. Immunobarnaznye kon’yugaty dlya diagnostiki i terapii raka. (Immunobarnase conjugates for diagnosis and treatment of cancer.) [dissertation] Moscow; 2010. 24 p. (In Russ)]
  67. Эдельвейс Э.Ф., Баландин Т.Г., Стремовский О.А. и др. Иммуноконъюгат анти-EGFR-мини-антитело–барназа высокотоксичен для опухолевых клеток человека. Доклады Академии наук. 2010;434(4):558–61.
    [Edel’veis EF, Balandin TG, Stremovskii OA, et al. Anti-anti-EGFR–barnase immunoconjugate is highly toxic for human tumor cells. Doklady Akademii nauk. 2010;434(4):558–61. (In Russ)]
  68. Schirrmann T, Krauss J, Arndt MA, et al. Targeted therapeutic RNases (ImmunoRNases). Expert Opin Biol Ther. 2009;9:79–95. doi: 10.1517/14712590802631862.
  69. De Lorenzo C, Arciello A, Cozzolino R, et al. A fully human antitumor immunoRNase selective for ErbB-2-positive carcinomas. Cancer Res. 2004;64(14):4870–4. doi: 10.1158/0008-5472.can-03-3717.
  70. De Lorenzo C, Tedesco A, Terrazzano G, et al. A human, compact, fully functional anti-ErbB2 antibody as a novel antitumour agent. Br J Cancer. 2004;91(6):1200–4. doi: 10.1038/sj.bjc.6602110.
  71. Покровский В.С., Трещалина Е.М. Ферментные препараты в онкогематологии: актуальные направления экспериментальных исследований и перспективы клинического применения. Клиническая онкогематология. 2014;7(1):28–39.
    [Pokrovskii VS, Treshchalina EM. Enzymes in oncohaematology: relevant directions of experimental studies and prospects of clinical use. Klinicheskaya onkogematologiya. 2014;7(1):28–39. (In Russ)]
  72. Покровский В.С., Лесная Н.А., Трещалина Е.М. и др. Перспективы разработки новых ферментных противоопухолевых препаратов. Вопросы онкологии. 2011;57(2):155–64.
    [Pokrovskii VS, Lesnaya NA, Treshchalina EM, et al. Perspectives of development of novel enzymatic antitumor agents. Voprosy onkologii. 2011;57(2):155–64. (In Russ)]
  73. Hatlen MA, Wang L, Nimer SD. AML1-ETO driven acute leukemia: insights into pathogenesis and potential therapeutic approaches. Front Med. 2012;6(3):248–62. doi: 10.1007/s11684-012-0206-6.
  74. Ziai JM, Siddon AJ, et al. Pathology Consultation on Gene Mutations in Acute Myeloid Leukemia. Am J Clin Pathol. 2015;144(4):539–54. doi: 10.1309/AJCP77ZFPUQGYGWY.