Siramesine triggers cell death through destabilisation of mitochondria, but not lysosomes

Cell Death and Disease

Volumn 4, Issue 10, 2013, Pages

  Hafner Cesen M ^a   Repnik, U ^a,b   Turk, V ^a   Turk, B ^a,c  

^a JO EF STEFAN INSTITUTE   (Slovenia)

^b UNIVERSITY OF OSLO   (Norway)

^c Center of Excellence CIPKEBIP   (Slovenia)

Author keywords

Apoptosis; Cell death; Lysosome; Mitochondria; Siramesine

Indexed keywords

ACETYLCYSTEINE; ALPHA TOCOPHEROL; CARDIOLIPIN; CASPASE; CATHEPSIN; CYTOCHROME C; LYSOSOME ENZYME; SIRAMESINE;

APOPTOSIS; ARTICLE; CELL DEATH; CELL STRUCTURE; CELL VIABILITY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOSOL; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; ENERGY BALANCE; ENZYME ACTIVATION; ENZYME RELEASE; HUMAN; HUMAN CELL; LIPID PEROXIDATION; LYSOSOME; LYSOSOME MEMBRANE; MEMBRANE PERMEABILITY; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; PH; PRIORITY JOURNAL;

CATHEPSIN L; CELL DEATH; CELL LINE, TUMOR; ENDOPLASMIC RETICULUM; HUMANS; INDOLES; INTRACELLULAR MEMBRANES; LYSOSOMES; MEMBRANE FUSION; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICROTUBULE-ASSOCIATED PROTEINS; MITOCHONDRIA; PERMEABILITY; PHAGOSOMES; REACTIVE OXYGEN SPECIES; SPIRO COMPOUNDS;

EID: 84887473756     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2013.361     Document Type: Article

References (43)

1. Martin WR, Eades CG, Thompson JA, Huppler RE, Gilbert PE. The effects of morphineand nalorphine- like drugs in the nondependent and morphine-dependent chronic spinal dog. J Pharmacol Exp Ther 1976; 197: 517-532.
2. Quirion R, Bowen WD, Itzhak Y, Junien JL, Musacchio JM, Rothman RB et al. A proposal for the classification of sigma binding sites. Trends Pharmacol Sci 1992; 13: 85-86.
3. Hellewell SB, Bowen WD. A sigma-like binding site in rat pheochromocytoma (PC12) cells: Decreased affinity for (+)-benzomorphans and lower molecular weight suggest a different sigma receptor form from that of guinea pig brain. Brain Res 1990; 527: 244-253.
4. Colabufo NA, Berardi F, Contino M, Niso M, Abate C, Perrone R et al. Antiproliferative and cytotoxic effects of some sigma2 agonists and sigma1 antagonists in tumour cell lines. Naunyn Schmiedebergs Arch Pharmacol 2004; 370: 106-113.
5. Spruce BA, Campbell LA, McTavish N, Cooper MA, Appleyard MV, O'Neill M et al. Small molecule antagonists of the sigma-1 receptor cause selective release of the death program in tumor and self-reliant cells and inhibit tumor growth in vitro and in vivo. Cancer Res 2004; 64: 4875-4886.
6. Crawford KW, Bowen WD. Sigma-2 receptor agonists activate a novel apoptotic pathway and potentiate antineoplastic drugs in breast tumor cell lines. Cancer Res 2002; 62: 313-322.
7. Hornick JR, Vangveravong S, Spitzer D, Abate C, Berardi F, Goedegebuure P et al. Lysosomal membrane permeabilization is an early event in sigma-2 receptor ligand mediated cell death in pancreatic cancer. J Exp Clin Cancer Res 2012; 31: 41.
8. Jonhede S, Petersen A, Zetterberg M, Karlsson JO. Acute effects of the sigma-2 receptor agonist siramesine on lysosomal and extra-lysosomal proteolytic systems in lens epithelial cells. Mol Vis 2010; 16: 819-827.
9. Ostenfeld MS, Fehrenbacher N, Hoyer-Hansen M, Thomsen C, Farkas T, Jaattela M. Effective tumor cell death by sigma-2 receptor ligand siramesine involves lysosomal leakage and oxidative stress. Cancer Res 2005; 65: 8975-8983.
10. Zeng C, Rothfuss J, Zhang J, Chu W, Vangveravong S, Tu Z et al. Sigma-2 ligands induce tumour cell death by multiple signalling pathways. Br J Cancer 2012; 106: 693-701.
11. Bem WT, Thomas GE, Mamone JY, Homan SM, Levy BK, Johnson FE et al. Overexpression of sigma receptors in nonneural human tumors. Cancer Res 1991; 51: 6558-6562.
12. Vilner BJ, John CS, Bowen WD. Sigma-1 and sigma-2 receptors are expressed in a wide variety of human and rodent tumor cell lines. Cancer Res 1995; 55: 408-413.
13. Walker JM, Bowen WD, Walker FO, Matsumoto RR, De Costa B, Rice KC. Sigma receptors: Biology and function. Pharmacol Rev 1990; 42: 355-402.
14. Banister SD, Kassiou M. The therapeutic potential of sigma (sigma) receptors for the treatment of central nervous system diseases: Evaluation of the evidence. Curr Pharm Des 2012; 18: 884-901.
15. Heading C. Siramesine H Lundbeck. Curr Opin Investig Drugs 2001; 2: 266-270.
16. Moltzen EK, Perregaard J, Meier E. Sigma ligands with subnanomolar affinity and preference for the sigma 2 binding site. 2. Spiro-joined benzofuran, isobenzofuran, and benzopyran piperidines. J Med Chem 1995; 38: 2009-2017.
17. Perregaard J, Moltzen EK, Meier E, Sanchez C. Sigma ligands with subnanomolar affinity and preference for the sigma 2 binding site. 1. 3-(omega-Aminoalkyl)-1 H-indoles. J Med Chem 1995; 38: 1998-2008.
18. Soby KK, Mikkelsen JD, Meier E, Thomsen C. Lu 28-179 labels a sigma(2)-site in rat and human brain. Neuropharmacology 2002; 43: 95-100.
19. Hornick JR, Xu J, Vangveravong S, Tu Z, Mitchem JB, Spitzer D et al. The novel sigma-2 receptor ligand SW43 stabilizes pancreas cancer progression in combination with gemcitabine. Mol Cancer 2010; 9: 298.
20. Ostenfeld MS, Hoyer-Hansen M, Bastholm L, Fehrenbacher N, Olsen OD, Groth-Pedersen L et al. Anti-cancer agent siramesine is a lysosomotropic detergent that induces cytoprotective autophagosome accumulation. Autophagy 2008; 4: 487-499.
21. Spirkoski J, Melo FR, Grujic M, Calounova G, Lundequist A, Wernersson S et al. Mast cell apoptosis induced by siramesine, a sigma-2 receptor agonist. Biochem Pharmacol 2012; 84: 1671-1680.
22. Cirman T, Oresic K, Droga-Mazovec G, Turk V, Reed JC, Myers RM et al. Selective disruption of lysosomes in HeLa cells triggers apoptosis mediated by cleavage of Bid by multiple papain-like lysosomal cathepsins. J Biol Chem 2004; 279: 3578-3587.
23. Droga-Mazovec G, Bojiç L, Petelin A, Ivanova S, Romih R, Repnik U et al. Cysteine cathepsins trigger caspase-dependent cell death through cleavage of bid and antiapoptotic Bcl-2 homologues. J Biol Chem 2008; 283: 19140-19150.
24. Grau A, Ortiz A. Dissimilar protection of tocopherol isomers against membrane hydrolysis by phospholipase A2. Chem Phys Lipids 1998; 91: 109-118.
25. Sadowska AM, Manuel YKB, De Backer WA. Antioxidant and anti-inflammatory efficacy of NAC in the treatment of COPD: Discordant in vitro and in vivo dose-effects: A review. Pulm Pharmacol Ther 2007; 20: 9-22.
26. Ivanova S, Repnik U, Bojiç L, Petelin A, Turk V, Turk B. Lysosomes in apoptosis. Methods Enzymol 2008; 442: 183-199.
27. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012; 8: 445-544.
28. Zeng C, Vangveravong S, Xu J, Chang KC, Hotchkiss RS, Wheeler KT et al. Subcellular localization of sigma-2 receptors in breast cancer cells using two-photon and confocal microscopy. Cancer Res 2007; 67: 6708-6716.
29. Abate C, Perrone R, Berardi F. Classes of sigma2 (sigma2) receptor ligands: Structure affinity relationship (SAfiR) studies and antiproliferative activity. Curr Pharm Des 2012; 18: 938-949.
30. Mamolo MG, Zampieri D, Zanette C, Florio C, Collina S, Urbano M et al. Substituted benzylaminoalkylindoles with preference for the sigma2 binding site. Eur J Med Chem 2008; 43: 2073-2081.
31. Kagan VE, Tyurin VA, Jiang J, Tyurina YY, Ritov VB, Amoscato AA et al. Cytochrome c acts as a cardiolipin oxygenase required for release of proapoptotic factors. Nat Chem Biol 2005; 1: 223-232.
32. Turk B, Turk V. Lysosomes as ''suicide bags'' in cell death: Myth or reality? J Biol Chem 2009; 284: 21783-21787.
33. Repnik U, HafnerÇ esen M, Turk B. The endolysosomal system in cell death and survival. Cold Spring Harb Perspect Biol 2013; 5: A008755.
34. Repnik U, Stoka V, Turk V, Turk B. Lysosomes and lysosomal cathepsins in cell death. Biochim Biophys Acta 2012; 1824: 22-33.
35. Vilner BJ, Bowen WD. Modulation of cellular calcium by sigma-2 receptors: Release from intracellular stores in human SK-N-SH neuroblastoma cells. J Pharmacol Exp Ther 2000; 292: 900-911.
36. Parry MJ, Alakoskela JM, Khandelia H, Kumar SA, Jaattela M, Mahalka AK et al. High-Affinity small molecule-phospholipid complex formation: Binding of siramesine to phosphatidic acid. J Am Chem Soc 2008; 130: 12953-12960.
37. Kooijman EE, Chupin V, de Kruijff B, Burger KN. Modulation of membrane curvature by phosphatidic acid and lysophosphatidic acid. Traffic 2003; 4: 162-174.
38. Kagan VE, Bayir HA, Belikova NA, Kapralov O, Tyurina YY, Tyurin VA et al. Cytochrome c/cardiolipin relations in mitochondria: A kiss of death. Free Radic Biol Med 2009; 46: 1439-1453.
39. Yang SB, Proks P, Ashcroft FM, Rupnik M. Inhibition of ATP-sensitive potassium channels by haloperidol. Br J Pharmacol 2004; 143: 960-967.
40. Cassano G, Gasparre G, Contino M, Niso M, Berardi F, Perrone R et al. The sigma-2 receptor agonist PB28 inhibits calcium release from the endoplasmic reticulum of SK-N-SH neuroblastoma cells. Cell Calcium 2006; 40: 23-28.
41. Monassier L, Manoury B, Bellocq C, Weissenburger J, Greney H, Zimmermann D et al. sigma(2)-receptor ligand-mediated inhibition of inwardly rectifying K(+) channels in the heart. J Pharmacol Exp Ther 2007; 322: 341-350.
42. Muench SP, Trinick J, Harrison MA. Structural divergence of the rotary ATPases. Q Rev Biophys 2011; 44: 311-356.
43. Nakanishi-Matsui M, Sekiya M, Nakamoto RK, Futai M. The mechanism of rotating proton pumping ATPases. Biochim Biophys Acta 2010; 1797: 1343-1352.