1,798
Views
8
CrossRef citations to date
0
Altmetric
Original Articles

Discovery and antitumor evaluation of novel inhibitors of spermine oxidase

, , , , , & show all
Pages 1140-1151 | Received 07 Nov 2018, Accepted 16 May 2019, Published online: 03 Jun 2019

References

  • Pegg AE, Casero RA, Jr. Current status of the polyamine research field. Methods Mol Biol 2011;720:3–35.
  • Amendola R, Cervelli M, Fratini E, et al. Spermine metabolism and anticancer therapy. Curr Cancer Drug Targets 2009;9:118–30.
  • Igarashi K, Kashiwagi K. Polyamines: mysterious modulators of cellular functions. Biochem Biophys Res Commun 2000;271:559–64.
  • Bachrach U. Naturally occurring polyamines: interaction with macromolecules. Curr Protein Pept Sci 2005;6:559–66.
  • Battaglia V, DeStefano Shields C, Murray-Stewart T, Casero RA, Jr. Polyamine catabolism in carcinogenesis: potential targets for chemotherapy and chemoprevention. Amino Acids 2014;46:511–19.
  • Schipper RG, Penning LC, Verhofstad AA. Involvement of polyamines in apoptosis. Facts and controversies: effectors or protectors? Semin Cancer Biol 2000;10:55–68.
  • Casero RA, Jr, Murray Stewart T, Pegg AE. Polyamine metabolism and cancer: treatments, challenges and opportunities. Nat Rev Cancer 2018;18:681–95.
  • Casero RA, Jr, Marton LJ. Targeting polyamine metabolism and function in cancer and other hyperproliferative diseases. Nat Rev Drug Discov 2007;6:373–90.
  • Babbar N, Murray-Stewart T, Casero RA, Jr. Inflammation and polyamine catabolism: the good, the bad and the ugly. Biochem Soc Trans 2007;35:300–4.
  • Park MH, Igarashi K. Polyamines and their metabolites as diagnostic markers of human diseases. Biomol Ther (Seoul) 2013;21:1–9.
  • Igarashi K, Kashiwagi K. Protein-conjugated acrolein as a biochemical marker of brain infarction. Mol Nutr Food Res 2011;55:1332–41.
  • Igarashi K, Ueda S, Yoshida K, Kashiwagi K. Polyamines in renal failure. Amino Acids 2006;31:477–83.
  • Kramer DL, Diegelman P, Jell J, et al. Polyamine acetylation modulates polyamine metabolic flux, a prelude to broader metabolic consequences. J Biol Chem 2008;283:4241–51.
  • Pegg AE. Functions of polyamines in mammals. J Biol Chem 2016;291:14904–12.
  • Khomutov MA, Weisell J, Hyvonen M, et al. Hydroxylamine derivatives for regulation of spermine and spermidine metabolism. Biochemistry (Mosc) 2013;78:1431–46.
  • Kee K, Vujcic S, Merali S, et al. Metabolic and antiproliferative consequences of activated polyamine catabolism in LNCaP prostate carcinoma cells. J Biol Chem 2004;279:27050–8.
  • Nowotarski SL, Woster PM, Casero RA, Jr. Polyamines and cancer: implications for chemotherapy and chemoprevention. Expert Rev Mol Med 2013;15:e3.
  • Wang Y, Hacker A, Murray-Stewart T, et al. Induction of human spermine oxidase SMO(PAOh1) is regulated at the levels of new mRNA synthesis, mRNA stabilization and newly synthesized protein. Biochem J 2005;386:543–7.
  • Wang Y, Devereux W, Woster PM, et al. Cloning and characterization of a human polyamine oxidase that is inducible by polyamine analogue exposure. Cancer Res 2001;61:5370–3.
  • Cervelli M, Salvi D, Polticelli F, et al. Structure-function relationships in the evolutionary framework of spermine oxidase. J Mol Evol 2013;76:365–70.
  • Murray-Stewart T, Wang Y, Goodwin A, et al. Nuclear localization of human spermine oxidase isoforms - possible implications in drug response and disease etiology. FEBS J 2008;275:2795–806.
  • Cervelli M, Amendola R, Polticelli F, Mariottini P. Spermine oxidase: ten years after. Amino Acids 2012;42:441–50.
  • Xu H, Chaturvedi R, Cheng Y, et al. Spermine oxidation induced by Helicobacter pylori results in apoptosis and DNA damage: implications for gastric carcinogenesis. Cancer Res 2004;64:8521–5.
  • Hong SK, Chaturvedi R, Piazuelo MB, et al. Increased expression and cellular localization of spermine oxidase in ulcerative colitis and relationship to disease activity. Inflamm Bowel Dis 2010;16:1557–66.
  • Goodwin AC, Jadallah S, Toubaji A, et al. Increased spermine oxidase expression in human prostate cancer and prostatic intraepithelial neoplasia tissues. Prostate 2008;68:766–72.
  • Smirnova OA, Keinanen TA, Ivanova ON, et al. Hepatitis C virus alters metabolism of biogenic polyamines by affecting expression of key enzymes of their metabolism. Biochem Biophys Res Commun 2017;483:904–9.
  • Chaturvedi R, de Sablet T, Peek RM, Wilson KT. Spermine oxidase, a polyamine catabolic enzyme that links Helicobacter pylori CagA and gastric cancer risk. Gut Microbes 2012;3:48–56.
  • Pledgie A, Huang Y, Hacker A, et al. Spermine oxidase SMO(PAOh1), Not N1-acetylpolyamine oxidase PAO, is the primary source of cytotoxic H2O2 in polyamine analogue-treated human breast cancer cell lines. J Biol Chem 2005;280:39843–51.
  • Parsonnet J, Friedman GD, Orentreich N, Vogelman H. Risk for gastric cancer in people with CagA positive or CagA negative Helicobacter pylori infection. Gut 1997;40:297–301.
  • Mastrantonio R, Cervelli M, Pietropaoli S, et al. HIV-Tat induces the Nrf2/ARE pathway through NMDA receptor-elicited spermine oxidase activation in human neuroblastoma cells. PLoS One 2016;11:e0149802.
  • Uemura T, Takasaka T, Igarashi K, Ikegaya H. Spermine oxidase promotes bile canalicular lumen formation through acrolein production. Sci Rep 2017;7:14841.
  • Hu T, Sun D, Zhang J, et al. Spermine oxidase is upregulated and promotes tumor growth in hepatocellular carcinoma. Hepatol Res 2018;48:967–77.
  • Vujcic S, Diegelman P, Bacchi CJ, et al. Identification and characterization of a novel flavin-containing spermine oxidase of mammalian cell origin. Biochem J 2002;367:665–75.
  • Wang Y, Murray-Stewart T, Devereux W, et al. Properties of purified recombinant human polyamine oxidase, PAOh1/SMO. Biochem Biophys Res Commun 2003;304:605–11.
  • Moriya S, Iwasaki K, Samejima K, et al. A mass spectrometric method to determine activities of enzymes involved in polyamine catabolism. Anal Chim Acta 2012;748:45–52.
  • Seiler N, Renault J, Gosse F, et al. Cytotoxicity of the polyamine oxidase inactivator MDL 72527 to cancer cells: comparison with a saturated structural analogue. Int J Oncol 2005;27:1669–76.
  • Grigorenko NA, Khomutov MA, Simonian AR, et al. Synthesis of 2,11-bis(methylidene)spermine, a new inhibitor of spermine oxidase. Russ J Bioorgan Chem 2016;42:423–7.
  • Cervelli M, Angelucci E, Stano P, et al. The Glu(2)(1)(6)/Ser(2)(1)(8) pocket is a major determinant of spermine oxidase substrate specificity. Biochem J 2014;461:453–9.
  • Bianchi M, Polticelli F, Ascenzi P, et al. Inhibition of polyamine and spermine oxidases by polyamine analogues. FEBS J 2006;273:1115–23.
  • Tavladoraki P, Cervelli M, Antonangeli F, et al. Probing mammalian spermine oxidase enzyme-substrate complex through molecular modeling, site-directed mutagenesis and biochemical characterization. Amino Acids 2011;40:1115–26.
  • Cervelli M, Bellavia G, Fratini E, et al. Spermine oxidase (SMO) activity in breast tumor tissues and biochemical analysis of the anticancer spermine analogues BENSpm and CPENSpm. BMC Cancer 2010;10:555.
  • Murray-Stewart TR, Woster PM, Casero RA, Jr. Targeting polyamine metabolism for cancer therapy and prevention. Biochem J 2016;473:2937–53.
  • Kaserer T, Beck KR, Akram M, et al. Pharmacophore models and pharmacophore-based virtual screening: concepts and applications exemplified on hydroxysteroid dehydrogenases. Molecules 2015;20:22799–832.
  • Yunlan L, Juan Z, Qingshan L. Antitumor activity of di-n-butyl-(2,6-difluorobenzohydroxamato)tin(IV) against human gastric carcinoma SGC-7901 cells via G2/M cell cycle arrest and cell apoptosis. PLoS One 2014;9:e90793.
  • Adams JM, Cory S. The Bcl-2 protein family: arbiters of cell survival. Science 1998;281:1322–6.
  • Li Y, Liu J, Li Q. Mechanisms by which the antitumor compound di-n-butyl-di-(4-chlorobenzohydroxamato)tin(IV) induces apoptosis and the mitochondrial-mediated signaling pathway in human cancer SGC-7901 cells. Mol Carcinog 2010;49:566–81.
  • Erdélyi P, Borsos E, Takács-Vellai K, et al. Shared developmental roles and transcriptional control of autophagy and apoptosis in Caenorhabditis elegans. J Cell Sci 2011;124:1510–8.
  • Nakagawa S, Ueno T, Manabe T, Kawasaki K. Imidazolines increase the levels of the autophagosomal marker LC3-II in macrophage-like RAW264.7 cells. Can J Physiol Pharmacol 2018;96:845–9.
  • Duran A, Amanchy R, Linares JF, et al. p62 is a key regulator of nutrient sensing in the mTORC1 pathway. Mol Cell 2011;44:134–46.