Divergent regulation of the key enzymes of polyamine metabolism by chiral α-methylated polyamine analogues

Biochemical Journal

Volumn 422, Issue 2, 2009, Pages 321-328

  Hyvönen, Mervi T ^a   Howard, Michael T ^b   Anderson, Christine B ^b   Grigorenko, Nikolay ^c   Khomutov, Alex R ^c   Vepsäläinen, Jouko ^a   Alhonen, Leena ^a   Jänne, Juhani ^a   Keinänen, Tuomo A ^a  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^c ENGELHARDT INSTITUTE OF MOLECULAR BIOLOGY   (Russian Federation)

Author keywords

Alternative splicing; Difluoromethylornithine; Frameshifting; Optical isomer; Polyamines; Uupstream open reading frame

Indexed keywords

ALTERNATIVE SPLICING; DIFLUOROMETHYLORNITHINE; FRAMESHIFTING; OPTICAL ISOMER; POLYAMINES; UUPSTREAM OPEN READING FRAME;

BIOCHEMISTRY; CATALYSTS; CELL PROLIFERATION; ENZYME INHIBITION; ENZYMES; ISOMERS; METABOLISM; STEREOCHEMISTRY;

AMINES;

ADENOSYLMETHIONINE DECARBOXYLASE; ANTIZYME; EFLORNITHINE; MESSENGER RNA; ORNITHINE DECARBOXYLASE; POLYAMINE; POLYAMINE DERIVATIVE; PUTRESCINE; SPERMIDINE DERIVATIVE; SPERMINE; 1 METHYLSPERMIDINE; 1-METHYLSPERMIDINE; DRUG DERIVATIVE; ENZYME; SPERMIDINE;

ALTERNATIVE RNA SPLICING; ARTICLE; CATALYSIS; CELL STRAIN HEK293; CHIRALITY; CONTROLLED STUDY; DOWN REGULATION; ENANTIOMER; ENZYME ACTIVITY; ENZYME REGULATION; HUMAN; HUMAN CELL; ISOMER; METHYLATION; OPEN READING FRAME; POLYAMINE METABOLISM; POLYAMINE SYNTHESIS; PRIORITY JOURNAL; REGULATORY MECHANISM; RIBOSOMAL FRAMESHIFTING; STEREOISOMERISM; TRANSLATION REGULATION; ANIMAL; CELL CULTURE; CELL LINE; CHEMISTRY; COMPARATIVE STUDY; DNA METHYLATION; DOSE RESPONSE; DRUG EFFECT; GENETICS; METABOLISM; MOUSE; SYNTHESIS; TUMOR CELL LINE;

ANIMALS; CELL LINE; CELL LINE, TUMOR; CELLS, CULTURED; DNA METHYLATION; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYMES; HUMANS; MICE; POLYAMINES; SPERMIDINE; STEREOISOMERISM;

EID: 70149120949     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20090737     Document Type: Article

References (40)

1. Tabor, C. W. and Tabor, H. (1984) Polyamines. Annu. Rev. Biochem. 53, 749-790
2. Metcalf, B. W., Bey, R, Danzin, C., Jung, M. J., Casara, P. and Vevert, J. P. (1978) Catalytic irreversible inhibition of mammalian ornithine decarboxylase (E.C.4.1.1.17) by substrate and product analogues. J. Am. Chem. Soc. 100, 2551-2553
3. Williams-Ashman, H. G. and Schenone, A. (1972) Methyl glyoxal bis(guanylhydrazone) as a potent inhibitor of mammalian and yeast S-adenosymethionine decarboxylases. Biochem. Biophys. Res. Commun. 46, 288-295
4. Casara, P., Marchal, P., Wagner, J. and Danzin, C. (1989) 5′-{[(Z)-4-amino-2-butenyl]melthylamino}-5′-deoxyadenosine: a potent enzyme-activated irreversible inhibitor of S-adenosyl-L-methionione decarboxylase from Escherichia coli. J. Am. Chem. Soc. 111, 9111-9113
5. Wolff, A. C., Armstrong, D. K., Fetting, J. H., Carducci, M. K., Riley, C. D., Bender, J. F., Casero, Jr. R. A. and Davidson, N. E. (2003) A phase II study of the polyamine analog N1,N11-diethylnorspermine (DENSpm) daily for five days every 21 days in patients with previously treated metastatic breast cancer. Clin. Cancer Res. 9, 5922-5928
6. Simoneau, A. R., Gerner, E. W., Nagle, R., Ziogas, A., Fujikawa-Brooks, S., Yerushalmi, H., Ahlering, T. E., Lieberman, R., McLaren, C. E., Anton-Culver, H. and Meyskens, Jr, F. L. (2008) The effect of difluoromethylornithine on decreasing prostate size and polyamines in men: Results of a year-long phase IIb randomized placebo-controlled chemoprevention trial. Cancer Epidemiol. Biomarkers Prev. 17, 292-299
7. Hahm, H. A., Effinger, D. S., Bowling, K., Hoker, B., Chen, T. L., Zabelina, Y. and Casero, Jr, R. A. (2002) Phase I study of N(1),N(11)-diethylnorspermine in patients with non-small cell lung cancer. Clin. Cancer Res. 8, 684-690
8. Meyskens, Jr, F. L. and Gerner, E. W. (1999) Development of difluoromethylornithine (DFMO) as a chemoprevention agent. Clin. Cancer Res. 5, 945-951
9. Matsufuji, S., Matsufuji, I., Miyazaki, Y., Murakami, Y., Atkins, J. F., Gesteland. R. F. and Hayashi, S. (1995) Autoregulatory frameshitting in decoding mammalian ornithine decarboxylase antizyme. Cell 80, 51-60
10. Rom, E. and Kahana, C. (1994) Polyamines regulate the expression of ornithine decarboxylase antizyme in vitro by inducing ribosomal frame-shifting. Proc. Natl. Acad. Sci. U.S.A. 91, 3959-3963
11. Balasundaram, D., Dinman, J. D., Wickner, R. B., Tabor, C. W. and Tabor, H. (1994) Spermidine deficiency increases +1 ribosomal frameshifting efficiency and inhibits Ty1 retrotransposition in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A. 91. 172-176
12. Mitchell, J. L., Judd, G. G., Bareyal-Leyser, A. and Ling, S. Y. (1994) Feedback repression of polyamine transport is mediated by antizyme in mammalian tissue-culture cells. Biochem. J. 299, 19-22
13. Suzuki, T., He, Y., Kashiwagi, K., Murakami, Y., Hayashi, S. and Igarashi, K. (1994) Antizyme protects against abnormal accumulation and toxicity of polyamines in ornithine decarboxylase-overproducing cells. Proc. Natl. Acad. Sci. U.S.A. 91, 8930-8934
14. Ruan, H., Shantz, L. M., Pegg, A. E. and Morris, D. R. (1996) The upstream open reading frame of the mRNA encoding S-adenosylmethionine decarboxylase is a polyamine-responsive translational control element. J. Biol. Chem. 271, 29576-29582
15. Hyvönen, M. T., Uimari, A., Keinänen, T. A., Heikkinen, S., Pellinen, R., Wahlfors, T., Korhonen, A., Narvanen, A., Wahlfors, J., Alhonen, L. and Jänne, J. (2006) Polyamine-regulated unproductive splicing and translation of spermidine/spermine N1-acetyltransterase. RNA 12, 1569-1582
16. Lakanen, J. R., Coward, J. K. and Pegg, A. E. (1992) Alpha-methyl polyamines: Metabolically stable spermidine and spermine mimics capable of supporting growth in cells depleted of polyamines. J. Med. Chem. 35, 724-734
17. Järvinen, A., Grigorenko, N., Khomutov, A. R., Hyvönen, M. T., Uimari, A., Vepsäläinen, J., Sinervirta, R., Keinänen, T. A., Vujcic, S., Alhonen, L. et al. (2005) Metabolic stability of alpha-methylated polyamine derivatives and their use as substitutes for the natural polyamines. J. Biol. Chem. 280, 6595-6601
18. Keinänen, T. A., Järvinen, A., Uimari, A., Vepsäläinen, J., Khomutov, A. R., Grigorenko, N. A., Hyvönen, M. T., Cerrada-Gimenez, M., Alhonen, L. and Jänne, J. (2007) Alpha-methylated polyamines as potential drugs and experimental tools in enzymology. Mini Rev. Med. Chem. 7, 813-820
19. Järvinen, A. J., Cerrada-Gimenez, M., Grigorenko, N. A., Khomutov, A. R., Vepsäläinen, J. J., Sinervirta, R. M., Keinänen, T. A., Alhonen, L. I. and Jänne, J. E. (2006) Alpha-methyl polyamines: efficient synthesis and tolerance studies in vivo and in vitro. First evidence for dormant stereospecificity of polyamine oxidase. J. Med. Chem. 49, 399-406
20. Hyvönen, M. T., Keinänen, T. A., Cerrada-Gimenez, M., Sinervirta, R., Grigorenko, N., Khomutov, A. R., Vepsäläinen, J., Alhonen, L. and Jänne, J. (2007) Role of hypusinated eukaryotic translation initiation factor 5A in polyamine depletion-induced cytostasis. J. Biol. Chem. 282, 34700-34706
21. Alhonen, L., Karppinen, A., Uusi-Oukari, M., Vujcic, S., Korhonen, V. P., Halmekytö, M., Kramer, D. L., Hines, R., Jänne, J. and Porter, C. W. (1998) Correlation of polyamine and growth responses to N1,N11-diethylnorspermine in primary fetal fibroblasts derived from transgenic mice overexpressing spermidine/spermine N1-acetyltransferase. J. Biol. Chem. 273, 1964-1969
22. Grigorenko, N., Khomutov, A. R., Keinänen, T. A., Järvinen, A., Alhonen, L., Jänne, J. and Vepsäläinen, J. (2007) Synthesis of novel optical isomers of alpha-methylpolyamines. Tetrahedron 63, 2257-2262
23. Hyvönen, T., Keinänen, T. A., Khomutov, A. R., Khomutov, R. M. and Eloranta, T. O. (1992) Monitoring of the uptake and metabolism of aminooxy analogues of polyamines in cultured cells by high-performance liquid chromatography. J. Chromatogr. 574, 17-21
24. Giles, K. W. and Myers, A. (1965) An improved diphenylamine method for the estimation of deoxyribonucleic acid. Nature. 206, 93-93
25. Jänne, J. and Williams-Ashman, H. G. (1971) On the purification of L-ornithine decarboxylase from rat prostate and effects of thiol compounds on the enzyme. J. Biol. Chem. 246, 1725-1732
26. Bernacki, R. J., Bergeron, R. J. and Porter, C. W. (1992) Antitumor activity of N,N'-bis(ethyl)spermine homologues against human MALME-3 melanoma xenografts. Cancer Res. 52, 2424-2430
27. Petros, L. M., Graminski, G. F., Robinson, S., Burns, M. R., Kisiel, N., Gesteland, R. F., Atkins, J. F., Kramer, D. L., Howard, M. T. and Weeks, R. S. (2006) Polyamine analogs with xylene rings induce antizyme frameshitting, reduce ODC activity, and deplete cellular polyamines. J. Biochem. 140, 657-666
28. Grentzmann, G., Ingram, J. A., Kelly, P. J., Gesteland, R. F. and Atkins, J. F. (1998) A dual-luciferase reporter system for studying recoding signals. RNA 4, 479-486
29. Howard, M. T., Shirts, B. H., Zhou, J., Carlson, C. L., Matsufuji, S., Gesteland, R. F., Weeks, R. S. and Atkins, J. F. (2001) Cell culture analysis of the regulatory frameshift event required for the expression of mammalian antizymes. Genes Cells 6, 931-941
30. Law. G. L., Raney, A., Heusner, C. and Morris, D. R. (2001) Polyamine regulation of ribosome pausing at the upstream open reading frame of S-adenosylmethionine decarboxylase. J. Biol. Chem. 276, 38036-38043
31. Park, M. H., Cooper, H. L. and Folk, J. E. (1981) Identification of hypusine, an unusual amino acid, in a protein from human lymphocytes and of spermidine as its biosynthetic precursor. Proc. Natl. Acad. Sci. U. S.A. 78, 2869-2873
32. Mitchell, J. L., Leyser, A., Holtorff, M. S., Bates, J. S., Frydman, B., Valasinas, A. L., Reddy, V. K. and Marton, L. J. (2002) Antizyme induction by polyamine analogues as a factor of cell growth inhibition. Biochem. J. 366, 663-671
33. Sakata, K., Kashiwagi, K. and Igarashi, K. (2000) Properties of a polyamine transporter regulated by antizyme. Biochem. J. 347, 297-303
34. Higashi, K., Terui, Y., Inomata, E., Katagiri, D., Nomura, Y., Someya, T., Nishimura, K., Kashiwagi, K., Kawai, G. and Igarashi, K. (2008) Selective structural change of bulged-out region of double-stranded RNA containing bulged nucleotides by spermidine. Biochem. Biophys. Res. Commun. 370, 572-577
35. Pankaskie, M. C., Abdel-Monem, M. M., Raina, A., Wang, T. and Foker, J. E. (1981) Inhibitors of polyamine biosynthesis. 9. Effects of S-adenosyl-L-methionine analogues on mammalian aminopropyltransferases in vitro and polyamine biosynthesis in transformed lymphocytes. J. Med. Chem. 24, 549-553
36. Qu. N., Ignatenko, N. A., Yamauchi, R, Stringer, D. E., Levenson, C., Shannon, P., Perrin, S. and Gerner, E. W. (2003) Inhibition of human ornithine decarboxylase activity by enandomers of difluoromethylomithine. Biochem. J. 375, 465-470
37. Byers, T. L., Ganem, B. and Pegg, A. E. (1992) Cytostasis induced in L1210 murine leukaemia cells by the S-adenosyl-L-methionine decarboxylase inhibitor 5′-([(Z)-4-amino-2-butenyl]methylamino)- 5′-deoxyadenosine may be due to hypusine depletion. Biochem. J. 287, 717-724
38. Byers, T. L., Wiest, L., Wechter, R. S. and Pegg, A. E. (1993) Effects of chronic 5′-([(Z)-4-amino-2-butenyllmethylamino)-5′-deoxy- adenosine (AbeAdo) treatment on polyamine and eIF-5A metabolism in AbeAdo-sensitive and -resistant L1210 murine leukaernia cells. Biochem. J. 290, 115-121
39. Pegg, A. E., Nagarajan, S., Naficy, S. and Ganem, B. (1991) Role of unsaturated derivatives of spermidine as substrates for spermine synthase and in supporting growth of SV-3T3 cells. Biochem. J. 274, 167-171
40. Pegg, A. E., Poulin, R. and Coward, J. K. (1995) Use of aminopropyltransferase inhibitors and of non-metabolizable analogs to study polyamine regulation and function. Int. J. Biochem. Cell Biol. 27, 425-442