Synthetic polyamines activating autophagy: Effects on cancer cell death

European Journal of Medicinal Chemistry

Volumn 67, Issue , 2013, Pages 359-366

  Minarini, Anna ^a   Zini, Maddalena ^b   Milelli, Andrea ^a   Tumiatti, Vincenzo ^a   Marchetti, Chiara ^a   Nicolini, Benedetta ^b   Falconi, Mirella ^b   Farruggia, Giovanna ^a   Cappadone, Concettina ^a   Stefanelli, Claudio ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

Autophagy; Cancer therapy; Oxidative stress; Polyamine analogs

Indexed keywords

METHOCTRAMINE; POLYAMINE DERIVATIVE;

ANTIOXIDANT ACTIVITY; ARTICLE; AUTOPHAGY; CANCER CELL; CELL DEATH; CYTOTOXICITY; HELA CELL; HUMAN; HUMAN CELL; MEMBRANE POTENTIAL; OXIDATIVE STRESS;

3,3′-DIHEXYLOXACARBOCYANINE IODIDE; ACIDIC VESICULAR ORGANELLES; ACRIDINE ORANGE; AO; ATG5; AUTOPHAGY; AUTOPHAGY GENE 5; AVOS; CANCER THERAPY; DCFDA; DENSPM; DFMO; DICHLOROFLUORESCEINE DIACETATE; DIMETHYLSULPHOXIDE; DIOC6; DMSO; N(1),N(11)-DIETHYLNORSPERMINE; N-ACETYLCYSTEINE; NAC; OXIDATIVE STRESS; POLYAMINE ANALOGS; TEM; TRANSMISSION ELECTRON MICROSCOPY; Α-DIFLUOROMETHYLORNITHINE;

ANTINEOPLASTIC AGENTS; AUTOPHAGY; CELL PROLIFERATION; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SCREENING ASSAYS, ANTITUMOR; HELA CELLS; HT29 CELLS; HUMANS; MOLECULAR STRUCTURE; NEOPLASMS; POLYAMINES; STRUCTURE-ACTIVITY RELATIONSHIP; TUMOR CELLS, CULTURED;

EID: 84882468371     PISSN: 02235234     EISSN: 17683254     Source Type: Journal    
DOI: 10.1016/j.ejmech.2013.06.044     Document Type: Article

References (44)

1. R.A. Casero Jr., P.M.Woster, Recent advances in the development of polyamine analogues as antitumor agents, J. Med. Chem. 52 (2009) 4551-4573.
2. A.E. Pegg, Mammalian polyamine metabolism and function, IUBMB Life 61 (2009) 880-894.
3. K. Igarashi, K. Kashiwagi, Modulation of cellular function by polyamines, Int. J. Biochem. Cell Biol. 42 (2010) 39-51.
4. F. Madeo, T. Eisenberg, S. Büttner, C. Ruckenstuhl, G. Kroemer, Spermidine: a novel autophagy inducer and longevity elixir, Autophagy 6 (2010) 160-162.
5. E.W. Gerner, F.L. Meyskens Jr., Polyamines and cancer: old molecules, new understanding, Nat. Rev. Cancer 4 (2004) 781-792. (Pubitemid 39331150)
6. R.A. Casero Jr., L.J. Marton, Targeting polyamine metabolism and function in cancer and other hyperproliferative diseases, Nat. Rev. Drug Discov. 6 (2007) 6373-6390.
7. H.M. Wallace, K. Niiranen, Polyamine analogues e an update, Amino Acids 33 (2007) 261-265.
8. S.K. Sharma, S. Hazeldine, M.L. Crowley, A. Hanson, R. Beattie, S. Varghese, T.M. Senanayake, A. Hirata, F. Hirata, Y. Huang, Y. Wu, N. Steinbergs, T. Murray-Stewart, I. Bytheway, R.A. Casero Jr., P.M. Woster, Polyamine-based small molecule epigenetic modulators, MedChemComm 3 (2012) 14-21.
9. M.L. Bolognesi, A. Minarini, R. Budriesi, S. Cacciaguerra, A. Chiarini, S. Spampinato, V. Tumiatti, C. Melchiorre, Universal template approach to drug design: polyamines as selective muscarinic receptor antagonists, J. Med. Chem. 41 (1998) 4150-4160. (Pubitemid 28483490)
10. C. Melchiorre, A. Antonello, R. Banzi, M.L. Bolognesi, A. Minarini, M. Rosini, V. Tumiatti, Polymethylene tetraamine backbone as template for the development of biologically active polyamines, Med. Res. Rev. 23 (2003) 200-233. (Pubitemid 36241098)
11. C. Melchiorre, M.L. Bolognesi, A. Minarini, M. Rosini, V. Tumiatti, Polyamines in drug discovery: from the universal template approach to the multitarget-directed ligand design strategy, J. Med. Chem. 53 (2010) 5906-5914.
12. A. Minarini, A. Milelli, V. Tumiatti, M. Rosini, M.L. Bolognesi, C. Melchiorre, Synthetic polyamines: an overview of their multiple biological activities, Amino Acids 38 (2010) 383-392.
13. C. Melchiorre, A. Minarini, P. Angeli, D. Giardinà, U. Gulini, W. Quaglia, Polymethylene tetraamines as muscarinic receptor probes, Trends Pharmacol. Sci. 10 (1989) 55-59. (Pubitemid 20004464)
14. M. Zini, C.L. Passariello, D. Gottardi, S. Cetrullo, F. Flamigni, C. Pignatti, A. Minarini, V. Tumiatti, A. Milelli, C. Melchiorre, C. Stefanelli, Cytotoxicity of methoctramine and methoctramine-related polyamines, Chem. Biol. Interact. 181 (2009) 409-416.
15. R. Saiki, Y. Yoshizawa, A. Minarini, A. Milelli, C. Marchetti, V. Tumiatti, T. Toida, K. Kashiwagi, K. Igarashi, In vitro and in vivo evaluation of polymethylene tetraamine derivatives as NMDA receptor channel blockers, Bioorg. Med. Chem. Lett. 23 (2013) 3901-3904.
16. C. Melchiorre, A. Minarini, W. Quaglia, V. Tumiatti, Methoctramine, Drug Future 14 (1989) 628-631. (Pubitemid 19201498)
17. A. Minarini, R. Budriesi, A. Chiarini, C. Melchiorre, V. Tumiatti, Further investigation on methoctramine-related tetraamines: effects of terminal N-substitution and of chain length separating the four nitrogens on M2 muscarinic receptor blocking activity, Farmaco 46 (1991) 1167-1178.
18. V. Tumiatti, V. Andrisano, R. Banzi, M. Bartolini, A. Minarini, M. Rosini, C. Melchiorre, Structure-activity relationships of acetylcholinesterase noncovalent inhibitorsbasedonapolyamine backbone.3. Effect of replacing the inner polymethylene chain with cyclic moieties, J.Med. Chem. 47 (2004) 6490-6498. (Pubitemid 39657311)
19. V. Tumiatti, A. Minarini, A. Milelli, M. Rosini, M. Buccioni, G. Marucci, C. Ghelardini, C. Bellucci, C. Melchiorre, Structure-activity relationships of methoctramine-related polyamines as muscarinic antagonist: effect of replacing the inner polymethylene chain with cyclic moieties, Bioorg. Med. Chem. 15 (2007) 2312-2321. (Pubitemid 46240917)
20. Y. Chen, D.L. Kramer, P. Diegelman, S. Vujcic, C.W. Porter, Apoptotic signaling in polyamine analogue-treated SK-MEL-28 human melanoma cells, Cancer Res. 61 (2001) 6437-6444. (Pubitemid 32783249)
21. L. Yang, J. Zhao, Y. Zhu, Z. Tian, C. Wang, Reactive oxygen species (ROS) accumulation induced by mononaphthalimide-spermidine leads to intrinsic and AIF-mediated apoptosis in HeLa cells, Oncol. Rep. 25 (2011) 1099-1107.
22. A. Milelli, V. Tumiatti, M. Micco, M. Rosini, G. Zuccari, L. Raffaghello, G. Bianchi, V. Pistoia, J. Fernando Díaz, B. Pera, C. Trigili, I. Barasoain, C. Musetti, M. Toniolo, C. Sissi, S. Alcaro, F. Moraca, M. Zini, C. Stefanelli, A. Minarini, Structure-activity relationships of novel substituted naphthalene diimides as anticancer agents, Eur. J. Med. Chem. 57 (2012) 417-428.
23. A.J. Palmer, H.M. Wallace, The polyamine transport system as a target for anticancer drug development, Amino Acids 38 (2010) 415-422.
24. R.H. Davis, J.L. Ristow, Uptake, intracellular binding, and excretion of polyamine during growth of Neurospora crassa, Arch. Biochem. Biophys. 271 (1989) 315-322. (Pubitemid 19145376)
25. D. Soulet, L. Covassin, M. Kaouass, R. Charest-Gaudreault, M. Audette, R. Poulin, Role of endocytosis in the internalization of spermidine-C(2)-BODIPY, a highly fluorescent probe of polyamine transport, Biochem. J. 367 (2002) 347-357. (Pubitemid 35216809)
26. I.N. Lavrik, A. Golks, P.H. Krammer, Caspases: pharmacological manipulation of cell death, J. Clin. Invest. 115 (2005) 2665-2672. (Pubitemid 41434390)
27. J.D. Robertson, S. Orrenius, B. Zhivotovsky, Nuclear events in apoptosis, J. Struct. Biol. 129 (2000) 346-358.
28. J.S. Long, K.M. Ryan, New frontiers in promoting tumour cell death: targeting apoptosis, necroptosis and autophagy, Oncogene 31 (2012) 5045-5060.
29. A. Notte, L. Leclere, C. Michiels, Autophagy as a mediator of chemotherapy-induced cell death in cancer, Biochem. Pharmacol. 82 (2011) 427-434.
30. S. Zhou, L. Zhao, M. Kuang, B. Zhang, Z. Liang, T. Yi, Y. Wei, X. Zhao, Autophagy in tumorigenesis and cancer therapy: Dr. Jekyll or Mr. Hyde? Cancer Lett. 23 (2012) 115-127.
31. T. Eisenberg, H. Knauer, A. Schauer, S. Büttner, C. Ruckenstuhl, D. Carmona- Gutierrez, J. Ring, S. Schroeder, C. Magnes, L. Antonacci, H. Fussi, L. Deszcz, R. Hartl, E. Schraml, A. Criollo, E. Megalou, D. Weiskopf, P. Laun, G. Heeren, M. Breitenbach, B. Grubeck-Loebenstein, E. Herker, B. Fahrenkrog, K.U. Fröhlich, F. Sinner, N. Tavernarakis, N. Minois, G. Kroemer, F. Madeo, Induction of autophagy by spermidine promotes longevity, Nat. Cell. Biol. 11 (2009) 1305-1314.
32. Y. Kabeya, N. Mizushima, T. Ueno, A. Yamamoto, T. Kirisako, T. Noda, E. Kominami, Y. Ohsumi, T. Yoshimori, LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing, EMBO J. 19 (2000) 5720-5728.
33. S. Shen, O. Kepp, G. Kroemer, The end of autophagic cell death? Autophagy 8 (2012) 1-3.
34. R.G. Carroll, S.J. Martin, Autophagy in multiple myeloma: what makes you stronger can also kill you, Cancer Cell 23 (2013) 425-426.
35. S. Yousefi, H.U. Simon, Apoptosis regulation by autophagy gene 5, Crit. Rev. Oncol. Hematol. 63 (2007) 241-244. (Pubitemid 47126867)
36. C. Stefanelli, F. Bonavita, I. Stanic', M. Mignani, A. Facchini, C. Pignatti, F. Flamigni, C.M. Caldarera, Spermine causes caspase activation in leukaemia cells, FEBS Lett. 437 (1998) 233-236.
37. S.Q. Xie, Q. Li, Y.H. Zhang, J.H. Wang, Z.H. Mei, J. Zhao, C.J. Wang, NPC-16, a novel naphthalimide-polyamine conjugate, induced apoptosis and autophagy in human hepatoma HepG2 cells and Bel-7402 cells, Apoptosis 16 (2011) 27-34.
38. A.M. Choi, S.W. Ryter, B. Levine, Autophagy in human health and disease, N. Engl. J. Med. 368 (2013) 651-662.
39. I. Stanic, A. Facchini, R.M. Borzì, R. Vitellozzi, C. Stefanelli, M.B. Goldring, C. Guarnieri, A. Facchini, F. Flamigni, Polyamine depletion inhibits apoptosis following blocking of survival pathways in human chondrocytes stimulated by tumor necrosis factor-alpha, J. Cell. Physiol. 206 (2006) 138-146. (Pubitemid 41740725)
40. C. Stefanelli, F. Bonavita, I. Stanic', G. Farruggia, E. Falcieri, I. Robuffo, C. Pignatti, C. Muscari, C. Rossoni, C. Guarnieri, C.M. Caldarera, ATP depletion inhibits glucocorticoid-induced thymocyte apoptosis, Biochem. J. 322 (1997) 909-917.
41. A. Andreani, S. Burnelli, M. Granaiola, A. Leoni, A. Locatelli, R. Morigi, M. Rambaldi, L. Varoli, N. Calonghi, C. Cappadone, G. Farruggia, M. Zini, C. Stefanelli, L. Masotti, N.S. Radin, R.H. Shoemaker, New antitumor imidazo [2,1-b]thiazole guanylhydrazones and analogues, J. Med. Chem. 51 (2008) 809-816. (Pubitemid 351304690)
42. C.L. Passariello, M. Zini, P.A. Nassi, C. Pignatti, C. Stefanelli, Upregulation of SIRT1 deacetylase in phenylephrine-treated cardiomyoblasts, Biochem. Biophys. Res. Commun. 407 (2011) 512-516.
43. P. Karna, S. Zughaier, V. Pannu, R. Simmons, S. Narayan, R. Aneja, Induction of reactive oxygen species-mediated autophagy by a novel microtubule-modulating agent, J. Biol. Chem. 285 (2010) 18737-18748.
44. C.L. Passariello, D. Gottardi, S. Cetrullo, M. Zini, G. Campana, B. Tantini, C. Pignatti, F. Flamigni, C. Guarnieri, C.M. Caldarera, C. Stefanelli, Evidence that AMP-activated protein kinase can negatively modulate ornithine decarboxylase activity in cardiac myoblasts, Biochim. Biophys. Acta 1823 (2012) 800-807.