Effect of polyamine metabolism inhibitors on Lewis lung carcinoma growth and metastasis

Aim:To study the influence of polyamine metabolism inhibitors on the growth, metastasis and ornithine decarboxylase (ODC) activity of Lewis lung carcinoma. Materials and Methods: Experiments were performed on female mice C57Bl/6 with Lewis lung carcinoma. Nω-hydroxy-nor-arginine (nor-NOHA) and α-dif...

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Published in:Experimental Oncology
Date:2015
Main Authors: Samoilenko, О.А., Milinevska, O.A., Karnaushenko, O.V., Shlyakhovenko, V.A., Zaletok, S.P.
Format: Article
Language:English
Published: Інститут експериментальної патології, онкології і радіобіології ім. Р.Є. Кавецького НАН України 2015
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Cite this:Effect of polyamine metabolism inhibitors on Lewis lung carcinoma growth and metastasis / О.А. Samoilenko, O.A. Milinevska, O.V. Karnaushenko, V.A. Shlyakhovenko, S.P. Zaletok // Experimental Oncology. — 2015. — Т. 37, № 2. — С. 151-153. — Бібліогр.: 20 назв. — англ.

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Digital Library of Periodicals of National Academy of Sciences of Ukraine
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author Samoilenko, О.А.
Milinevska, O.A.
Karnaushenko, O.V.
Shlyakhovenko, V.A.
Zaletok, S.P.
author_facet Samoilenko, О.А.
Milinevska, O.A.
Karnaushenko, O.V.
Shlyakhovenko, V.A.
Zaletok, S.P.
citation_txt Effect of polyamine metabolism inhibitors on Lewis lung carcinoma growth and metastasis / О.А. Samoilenko, O.A. Milinevska, O.V. Karnaushenko, V.A. Shlyakhovenko, S.P. Zaletok // Experimental Oncology. — 2015. — Т. 37, № 2. — С. 151-153. — Бібліогр.: 20 назв. — англ.
collection DSpace DC
container_title Experimental Oncology
description Aim:To study the influence of polyamine metabolism inhibitors on the growth, metastasis and ornithine decarboxylase (ODC) activity of Lewis lung carcinoma. Materials and Methods: Experiments were performed on female mice C57Bl/6 with Lewis lung carcinoma. Nω-hydroxy-nor-arginine (nor-NOHA) and α-difluoromethylornithine (DFMO) were used as arginase and ODC inhibitors, correspondently. Inhibition of tumor growth was calculated by comparison of tumor volume in the treated and control groups. The average number of metastases per animal in the group and the average volume of pulmonary metastases per animal in the group have been determined. Determination of ODC — the key enzyme of the polyamine synthesis — in the samples of experimental tumors was performed by method of Luqman S. Results: Administration of DFMO or it’s combination with nor-NOHA resulted in the decrease of tumor growth rate, number and volume of lung metastases and was accompanied with reduced ODC activity in tumor tissue. Сonclusion: Modifiers of polyamine metabolism may be considered as promising targeted cancer therapy. Key Words: Lewis lung carcinoma, metastases, polyamine metabolism, ornithine decarboxylase, α-difluoromethylornithine, Nωhydroxy-nor-arginine.
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fulltext Experimental Oncology 37, 151–153, 2015 (June) 151 EFFECT OF POLYAMINE METABOLISM INHIBITORS ON LEWIS LUNG CARCINOMA GROWTH AND METASTASIS О.А. Samoilenko*, O.A. Milinevska, O.V. Karnaushenko, V.A. Shlyakhovenko, S.P. Zaletok R.E. Kavetsky Institute of Experimental Pathology, Oncology and Radiobiology, NAS of Ukraine, Kyiv 03022, Ukraine Aim: To study the influence of polyamine metabolism inhibitors on the growth, metastasis and ornithine decarboxylase (ODC) activity of Lewis lung carcinoma. Materials and Methods: Experiments were performed on female mice C57Bl/6 with Lewis lung carcinoma. Nω-hydroxy-nor-arginine (nor-NOHA) and α-difluoromethylornithine (DFMO) were used as arginase and ODC inhibitors, correspondently. Inhibition of tumor growth was calculated by comparison of tumor volume in the treated and control groups. The average number of metastases per animal in the group and the average volume of pulmonary metastases per animal in the group have been determined. Determination of ODC — the key enzyme of the polyamine synthesis — in the samples of ex- perimental tumors was performed by method of Luqman S. Results: Administration of DFMO or it’s combination with nor-NOHA resulted in the decrease of tumor growth rate, number and volume of lung metastases and was accompanied with reduced ODC activity in tumor tissue. Сonclusion: Modifiers of polyamine metabolism may be considered as promising targeted cancer therapy. Key Words: Lewis lung carcinoma, metastases, polyamine metabolism, ornithine decarboxylase, α-difluoromethylornithine, Nω- hydroxy-nor-arginine. Polyamines (PA) — putrescine, spermidine and spermine — natural polycations, which play a crucial role in many fundamental biological processes: DNA replication, transcription, translation, membrane protein function, protein folding and others [1–6]. The level of PA largely vary during physiological and pathological processes (embryogenesis, ageing [7–9], regenera- tion, infections, malignant transformation [10, 11]). The increased level of PA in tumor growth is used as a marker for monitoring in course of a disease and efficiency of therapy [12–14]. Inhibition the level of PA by blocking the activity of the key enzyme for pu- trescine synthesis ornithine decarboxylase (ODC) — one of the most promising directions in the develop- ment of new approaches to the cancer treatment. PA metabolism is regulated at different levels by a com- plex system of enzymes, which are prima rily enzymes of PA synthesis and transformation. The modification of genes regulating PA metabolism by external factors, not studied enough. The aim of this work was to study the effect of inhibitors of PA metabolism on the growth and metastasis of experimental Lewis lung carcinoma in mice. MATERIALS AND METHODS Experiments were per formed on female C57Bl/6 mice 16.2–23 g. Tumor strain Lewis lung car- cinoma was obtained from National Bank of Cell Lines and Transplanted Tumors of R.E. Kavetsky Institute of Experimental Pathology, Oncology and Radiobio- logy, NAS of Ukraine (Kyiv, Ukraine). All experiments were conducted in accordance to international rules of work with laboratory animals [15]. Lewis lung car- cinoma transplanted intramuscularly into the shin of the right rear leg 3•105 tumor cells in a volume of 0.2 ml of sterile isotonic sodium chloride solution. Animals were kept on a normal diet with free access to water. Each treatment group had 3–6 animals, con- trol group — 4 mice. Inhibitors applied: arginase inhibitor — Nω- hydroxy-nor-arginine (nor-NOHA) (Cayman Chemical, USA), inhibitor of ODC — α-difluoromethylornithine — DFMO (Centre de Recherche Merrell International, 16 rue d’Ankara, 67084 Strasbourg Cedex, France). nor-NOHA prepared immediately before use and injected into the abdominal cavity of mice in a dose of 60 mg/kg (1.2 mg per mouse in 0.2 ml of isotonic so- dium chloride solution) starting 7 days after tumor trans- plantation. A comparative analysis was performed versus a group of non-treated tumor-bearing mice (control). In each treatment group, 5 injections of an inhibitor were made. Control animals injected with 0.2 ml of ste- rile isotonic sodium chloride solution. The volume of tumors registered throughout the experiment. The animals were decapitated 1 day after the last in- jection of the inhibitors that is 14th day, and on the 26th day after tumor transplantation. The kinetics of tumor growth evaluated by means of measuring tumor diameters. Inhibition of tumor growth was calculated by comparison of tumor vo lume in the treated and control groups. To assess the inten- sity of the process of metastasis was used the following criteria: the average number of pulmonary metasta- ses per animal in the group and the average volume of metastases per animal in the group. In these studies, the number and volume of lung metastases in un- treated animals and in animals treated as described above for the tumor growth delay studies were scored on day 26 post-tumor implant. The number and volume of metastases were counted in the transmitted light Submitted: January 23, 2015. *Correspondence: E-mail: a-samoilenko@ukr.net Abbreviations used: DFMO — alpha-difluoromethylornithine; nor- NOHA — Nω-hydroxy-nor-arginine; ODC — ornithine decarboxy- lase; PA — polyamines. Exp Oncol 2015 37, 2, 151–153 SHORT COMMUNICATIONS 152 Experimental Oncology 37, 151–153, 2015 (June) after removal of the lung, fixing it between the glass plates. Tumor volume was calculated by the formula: V = a2 · b · π/6, where a — short, b — longer diameter of tumor. The metastas is inhibition index (MII) was calculated by the formula: MII = ((Ac − Ae)/Ac) · 100, where Ac — the number of metastases to the lung in mice of the control group and Ae — the frequency of metastases in a treated group. Determination of the ODC activity in the samples of expe rimental tumors was performed by meth- od S. Luqman [16, 17]. The method is based on the fact that the correspon ding enzyme converts L-ornithine hydrochloride (substrate) to the yellow colored pu- trescine adduct soluble in pentanol, which measured by spectrophotometer. The statistic processing of obtained results was conducted with the help of Student’s t-criterion. The data were reported as the M ± m. RESULTS AND DISCUSSION Arginine is a precursor for ornithine which may be then converted into putrescine — the first partici- pant in metabolic transformations of PA [18]. It was found that DFMO — specific inhibitor of ODC — pre- vents progression of cancer cells in model systems [19]. L-arginine is a nonessential amino acid that plays a central role in several biological systems includ- ing the immune response. L-arginine is metabolized by arginase I and arginase II with farther creation of or- nithine [20]. In our experiments, the effect of PA syn- thesis inhibitors — DFMO and a competitive inhibitor of ornithine synthesis nor-NOHA — on the Lewis lung carcinoma growth has been performed. The results are presented in Fig. 1, Table 1. As can be seen, there is a significant inhibition of tu- mor growth begining of the eleventh day of the experi- ment. During the experiment, both inhibitors studied demonstrate inhibi ting activity (within 28–43%). In this regard, it was important to follow the changes in the dynamics of tumor growth that presented in Fig. 1. 0 1000 2000 3000 4000 5000 6000 11 13 15 18 20 22 24 26 Day after transplantation Tu m or v ol um e, V m m 3 Control Nor-NOHA DFMO DFMO+nor-NOHA * * * * Fig. 1. Lewis lung carcinoma gro wth in mice under the influence of inhibitors of PA metabolism. *Significant difference (p < 0.05) with each experimental group (excluding the DFMO + nor-NOHA group at the 11th day, see Table 1) Assessing the growth rate of the primary tumor node, it was found that average daily increase of tumor volume in the control group of animals within 9 days (11–20 days) was 497.2 ± 56.0 mm3. The use of both studied inhibitors and their combination led to a sig- nificant reduction in the rate of growth, t he latter was about 300 mm3 d uring the same time period. Signifi- cant difference in the impact on growth inhibition when using different inhibitors was not found (Fig. 2). Table 1. Inhibition of growth of Lewis lung carcinoma in mice under influ- ence of inhibitors of PA metabolism Groups Nu m be r of a ni m al s The volume of tumors, mm3 Inhibition, % 11th day 13th day 20th day 11th day 13th day 20th day Control 4 1067 ± 133 2123 ± 165 5542 ± 439 − − − nor-NOHA 5 690 ± 129* 1194 ± 163* 3163 ± 662* 35.3 43.0 43.0 DFMO 4 633 ± 114* 1534 ± 232* 3305 ± 461* 40.7 28.0 40.0 D F M O + nor-NOHA 3 754 ± 138 1439 ± 149* 3504 ± 281* 0 32.0 37.0 Note: *p < 0.05 as compared to control. 0 100 200 300 400 500 600 Control nor-NOHA DFMO DFMO + nor-NOHA Tu m or g ro wt h ra te , m m 3 /d ay Fig. 2. T he rate of tumor growth of Lewis lung carcinoma in mice during 11–20 days compared to control It is known that transplanted Lewis lung carcinoma refers to metastatic tumors, so anti-metastatic effect, as to this tumor strain, is an important indicator of antitu- mor effect. The results of the next section of experiments devoted to examining the influence of inhibitors of PA me- tabolism on the growth of lung metastases (Table 2). Table 2. E ffect of inhibitors of PA metabolism on the number and volume of metastases of Lewis lung carcinoma in mice (26th day) Groups Number of ani- mals The average number of metastases per 1 animal The average volume of metastases per 1 animal n MІІ, % mm3 МІІ, % Control 4 11.0 ± 2.2 − 160.1 ± 44.1 − nor-NOHA 5 16.6 ± 3.2 0 138.8 ± 44.2 0 DFMO 4 12.0 ± 0.7 0 9.8 ± 2.3* 94 DFMO + nor-NOHA 3 11.0 ± 2.3 0 11.9 ± 5.3* 93 Note: *p < 0.01 as compared to control. As it is seen, the number of metastases in the lungs of all treated mice did not differ versus control. At the same time, volume of the metastatic lesions in the DFMO and DFMO + nor-NOHA groups was near 90% less versus control. Taking in mind the importance of the ODC enzyme and PA synthesis for cell proliferation, the next sec- tion of research was devoted to study of ODC activity in the cells of Lewis lung cancer after the action of in- hibitors of PA metabolism. The experimental results are presented in Table 3. The data obtained show that ODC activity in the tumor increases during the tumor development. On 26th day of experiment, ODC activity in tumors in all treated groups Experimental Oncology 37, 151–153, 2015 (June) 153 was decreased versus control (see Table 3). It may be expected that inhibition of ODC activity is the main cause of inhibition of tumor growth. Our preclinical data indicate that DFMO in combination with inhibitors of ar- ginase has potential for chemoprevention of cancer and should be evaluated in other models and in combination with other drugs in anticipation of future clinical trials. Table 3. Effect of inhibitors of PA metabolism on ODC activity in cells of experimental Lewis lung carcinoma Groups Number of ani- mals 13th day 26th day ODC activity, A.U./mg pro- tein Inhi- bition, % ODC activity, A.U./mg protein Inhi- bition, % Control 4 0.034 ± 0.002 − 0.578 ± 0.070 − nor-NOHA 5 0.070 ± 0.012# 0 0.346 ± 0.046* 40 DFMO 4 0.010 ± 0.001# 0 0.355 ± 0.060** 39 DFMO + nor- NOHA 3 0.019 ± 0.001# 0 0.348 ± 0.050* 40 Note: #0.1 < p <0.25; *0.025 < p < 0.01; **0.01 < p < 0.005 as compared to control. REFERENCES 1. Igarashi K, Kashiwagi K. Protein-conjugated acrolein as a biochemical marker of brain infarction. Mol Nutr Food Res 2011; 55: 1332–41. 2. Lopatin AN, Makhina EN, Nichols CG. Potassium channel block by cytoplasmic polyamines as the mechanism of intrinsic rectification. Nature 1994; 372: 366–9. 3. Williams K. Modulation and block of ion chan- nels: a new biology of polyamines. Cell Signal 1997; 9: 1–13. 4. Ha HC, Sirisoma NS, Kuppusamy P, et al. The natural polyamine spermine functions directly as a free radical sca- venger. Proc Natl Acad Sci USA 1998; 95: 11140–5. 5. Kurata HT, Marton LJ, Nichols CG. The polyamine binding site in inward rectifier K+ channels. J Gen Physiol 2006; 127: 467–80. 6. Agostinelli E, Marques MP, Calheiros R, et al. Poly- amines: fundamental characters in chemistry and biology. Amino Acids 2010; 38: 393–403. 7. Liu P, Gupta N, Jing Y, et al. Age-related changes in polyamines in memory-associated brain structures in rats. Mol Neurosc 2008; 55: 789–96. 8. Gupta VK, Scheunemann L, Eisenberg T, et al. Restor- ing polyamines protects from age-induced memory impair- ment in an autophagy-dependent manner. Nat Neurosci 2013; 16: 1453–60. 9. Minois N, Carmona-Gutierrez D, Madeo F. Polyamines in aging and disease. Aging 2011; 3: 716–32. 10. Casero RA Jr, Marton LJ. Targeting polyamine me- tabolism and function in cancer and other hyperproliferative diseases. Nat Rev Drug Discov 2007; 6: 373–90. 11. Pegg AE, Casero RA Jr. Current status of the polyamine research field. Meth Mol Biol 2011; 720: 3–35. 12. Park MH, Igarashi K. Polyamines and their metabo- lites as diagnostic markers of human diseases. Biomol Ther 2013; 21: 1–9. 13. Kawakita M, Hiramatsu K. Diacetylated derivatives of spermine and spermidine as novel promising tumor markers. J Biochem 2006; 139: 315–22. 14. Hiramatsu K, Takahashi K, Yamaguchi T, et al. N(1),N(12)-Diacetylspermine as a sensitive and specific novel marker for early- and late-stage colorectal and breast cancers. Clin Cancer Res 2005; 11: 2986–90. 15. Council Directive 2010/63/EU of 22 September 2010 on the protection of animals used for scientific purposes. Official J Eur Commun 2010; L 276: 33–79. 16. Luqman S, Masood N, Srivastava S, et al. Modified spectrophotometric and methodical approach to find novel inhibitors of ornithine decarboxylase enzyme: a path through the maze. Protocol Exchange 2013; doi:10.1038/protex.2013.045. 17. Shlyakhovenko VA, Milinevska OA. Determination of ornithine decarboxylase activity. Lab Diagnostics 2014; 1: 36–38 (in Ukrainian). 18. Morris SM Jr. Recent advances in arginine metabo- lism: roles and regulation of the arginases. Br J Pharmacol 2009; 157: 922–30. 19. Mohammed A, Janakiram NB, Madka V, et al. Eflor- nithine (DFMO) prevents progression of pancreatic cancer by modulating ornithine decarboxylase signaling. Cancer Prev Res 2014; 7: 1198–209. 20. Albina JE, Caldwell MD, Henry WL, et al. Regula- tion of macrophage functions by L-arginine. J Exp Med 1989; 169: 1021–9. Copyright © Experimental Oncology, 2015
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institution Digital Library of Periodicals of National Academy of Sciences of Ukraine
issn 1812-9269
language English
last_indexed 2025-11-28T13:54:39Z
publishDate 2015
publisher Інститут експериментальної патології, онкології і радіобіології ім. Р.Є. Кавецького НАН України
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spelling Samoilenko, О.А.
Milinevska, O.A.
Karnaushenko, O.V.
Shlyakhovenko, V.A.
Zaletok, S.P.
2019-01-22T11:38:49Z
2019-01-22T11:38:49Z
2015
Effect of polyamine metabolism inhibitors on Lewis lung carcinoma growth and metastasis / О.А. Samoilenko, O.A. Milinevska, O.V. Karnaushenko, V.A. Shlyakhovenko, S.P. Zaletok // Experimental Oncology. — 2015. — Т. 37, № 2. — С. 151-153. — Бібліогр.: 20 назв. — англ.
1812-9269
https://nasplib.isofts.kiev.ua/handle/123456789/145472
Aim:To study the influence of polyamine metabolism inhibitors on the growth, metastasis and ornithine decarboxylase (ODC) activity of Lewis lung carcinoma. Materials and Methods: Experiments were performed on female mice C57Bl/6 with Lewis lung carcinoma. Nω-hydroxy-nor-arginine (nor-NOHA) and α-difluoromethylornithine (DFMO) were used as arginase and ODC inhibitors, correspondently. Inhibition of tumor growth was calculated by comparison of tumor volume in the treated and control groups. The average number of metastases per animal in the group and the average volume of pulmonary metastases per animal in the group have been determined. Determination of ODC — the key enzyme of the polyamine synthesis — in the samples of experimental tumors was performed by method of Luqman S. Results: Administration of DFMO or it’s combination with nor-NOHA resulted in the decrease of tumor growth rate, number and volume of lung metastases and was accompanied with reduced ODC activity in tumor tissue. Сonclusion: Modifiers of polyamine metabolism may be considered as promising targeted cancer therapy. Key Words: Lewis lung carcinoma, metastases, polyamine metabolism, ornithine decarboxylase, α-difluoromethylornithine, Nωhydroxy-nor-arginine.
en
Інститут експериментальної патології, онкології і радіобіології ім. Р.Є. Кавецького НАН України
Experimental Oncology
Short communications
Effect of polyamine metabolism inhibitors on Lewis lung carcinoma growth and metastasis
Article
published earlier
spellingShingle Effect of polyamine metabolism inhibitors on Lewis lung carcinoma growth and metastasis
Samoilenko, О.А.
Milinevska, O.A.
Karnaushenko, O.V.
Shlyakhovenko, V.A.
Zaletok, S.P.
Short communications
title Effect of polyamine metabolism inhibitors on Lewis lung carcinoma growth and metastasis
title_full Effect of polyamine metabolism inhibitors on Lewis lung carcinoma growth and metastasis
title_fullStr Effect of polyamine metabolism inhibitors on Lewis lung carcinoma growth and metastasis
title_full_unstemmed Effect of polyamine metabolism inhibitors on Lewis lung carcinoma growth and metastasis
title_short Effect of polyamine metabolism inhibitors on Lewis lung carcinoma growth and metastasis
title_sort effect of polyamine metabolism inhibitors on lewis lung carcinoma growth and metastasis
topic Short communications
topic_facet Short communications
url https://nasplib.isofts.kiev.ua/handle/123456789/145472
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