Increased apoptosis in cancer cells in vitro and in vivo by ceramides in transferrin-modified liposomes

Cancer Biology and Therapy

Volumn 13, Issue 1, 2012, Pages 50-60

  Koshkaryev, Alexander ^a   Piroyan, Aleksanr ^a   Torchilin, Vladimir P ^a  

^a NORTHEASTERN UNIVERSITY   (United States)

Author keywords

Apoptosis; Cathepsins; Ceramide; Liposomes; Lysosomes

Indexed keywords

CALCEIN; CATHEPSIN D; CERAMIDE; LIPOCORTIN 5; LIPOSOME; TRANSFERRIN; TRANSFERRIN MODIFIED LIPOSOME; TRANSFERRIN RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER CELL; CANCER INHIBITION; CELL SURFACE; COMPARATIVE STUDY; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; HELA CELL; LYSOSOME MEMBRANE; MOUSE; NONHUMAN; OVARY CARCINOMA; PROTEIN EXPRESSION; TUMOR XENOGRAFT; ANIMAL; CHEMISTRY; DISEASE MODEL; DRUG EFFECT; DRUG SCREENING; HUMAN; LYSOSOME; METABOLISM; NUDE MOUSE; OVARY TUMOR;

ANIMALS; APOPTOSIS; CERAMIDES; DISEASE MODELS, ANIMAL; FEMALE; FLOW CYTOMETRY; HELA CELLS; HUMANS; LIPOSOMES; LYSOSOMES; MICE; MICE, NUDE; MICROSCOPY, FLUORESCENCE; OVARIAN NEOPLASMS; TRANSFERRIN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84856384153     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.4161/cbt.13.1.18871     Document Type: Article

References (38)

1. Castino R, Demoz M, Isidoro C. Destination 'lysosome': a target organelle for tumour cell killing? J Mol Recognit 2003; 16:337-48; PMID:14523947; http:// dx.doi.org/10.1002/jmr.643
2. Kirkegaard T, Jaattela M. Lysosomal involvement in cell death and cancer. Biochim Biophys Acta 2009; 1793:746-54; PMID:18948147; http://dx.doi.org/10. 1016/j.bbamcr.2008.09.008
3. Turk B, Turk V. Lysosomes as "suicide bags" in cell death: myth or reality?. J Biol Chem 2009; 284:21783- 7; PMID:19473965; http://dx.doi.org/10.1074/jbc. R109.023820
4. Johansson AC, Appelqvist H, Nilsson C, Kagedal K, Roberg K, Ollinger K. Regulation of apoptosisassociated lysosomal membrane permeabilization. Apoptosis 2010; 15:527-40; PMID:20077016; http:// dx.doi.org/10.1007/s10495-009-0452-5
5. Boya P, Andreau K, Poncet D, Zamzami N, Perfettini JL, Metivier D, et al. Lysosomal membrane permeabilization induces cell death in a mitochondrion-dependent fashion. J Exp Med 2003; 197:1323-34; PMID: 12756268; http://dx.doi.org/10.1084/jem.20021952
6. Roberg K, Ollinger K. Oxidative stress causes relocation of the lysosomal enzyme cathepsin D with ensuing apoptosis in neonatal rat cardiomyocytes. Am J Pathol 1998; 152:1151-6; PMID:9588882
7. Roberg K, Kagedal K, Ollinger K. Microinjection of cathepsin d induces caspase-dependent apoptosis in fibroblasts. Am J Pathol 2002; 161:89-96; PMID: 12107093; http://dx.doi.org/10.1016/S0002-9440(10) 64160-0
8. Boya P, Kroemer G. Lysosomal membrane permeabilization in cell death. Oncogene 2008; 27:6434-51; PMID:18955971; http://dx.doi.org/10.1038/onc. 2008.310
9. Cirman T, Oresic K, Mazovec GD, 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; 279:3578-87; PMID:14581476; http:// dx.doi.org/10.1074/jbc.M308347200
10. Bidère N, Lorenzo HK, Carmona S, Laforge M, Harper F, Dumont C, et al. Cathepsin D triggers Bax activation, resulting in selective apoptosis-inducing factor (AIF) relocation in T lymphocytes entering the early commitment phase to apoptosis. J Biol Chem 2003; 278:31401-11; PMID:12782632; http://dx.doi. org/10.1074/jbc.M301911200
11. Agostinelli E, Tempera G, Dalla Vedova L, Condello M, Arancia G. MDL 72527 and spermine oxidation products induce a lysosomotropic effect and mitochondrial alterations in tumour cells. Biochem Soc Trans 2007; 35:343-8; PMID:17371275; http://dx.doi.org/ 10.1042/BST0350343
12. Nakashima S, Hiraku Y, Tada-Oikawa S, Hishita T, Gabazza EC, Tamaki S, et al. Vacuolar H+-ATPase inhibitor induces apoptosis via lysosomal dysfunction in the human gastric cancer cell line MKN-1. J Biochem 2003; 134:359-64; PMID:14561721; http://dx.doi. org/10.1093/jb/mvg153
13. Werneburg NW, Guicciardi ME, Bronk SF, Gores GJ. Tumor necrosis factor-alpha-associated lysosomal permeabilization is cathepsin B dependent. Am J Physiol Gastrointest Liver Physiol 2002; 283:G947- 56; PMID:12223355
14. Werneburg NW, Guicciardi ME, Bronk SF, Kaufmann SH, Gores GJ. Tumor necrosis factor-related apoptosisinducing ligand activates a lysosomal pathway of apoptosis that is regulated by Bcl-2 proteins. J Biol Chem 2007; 282:28960-70; PMID:17686764; http:// dx.doi.org/10.1074/jbc.M705671200
15. Schütze S, Machleidt T, Adam D, Schwandner R, Wiegmann K, Kruse ML, et al. Inhibition of receptor internalization by monodansylcadaverine selectively blocks p55 tumor necrosis factor receptor death domain signaling. J Biol Chem 1999; 274:10203-12; PMID:10187805; http://dx.doi.org/10.1074/jbc.274. 15.10203
16. Dumitru CA, Sandalcioglu IE, Wagner M, Weller M, Gulbins E. Lysosomal ceramide mediates gemcitabineinduced death of glioma cells. J Mol Med 2009; 87: 1123-32; PMID:19763526; http://dx.doi.org/10. 1007/s00109-009-0514-8
17. Kågedal K, Zhao M, Svensson I, Brunk UT. Sphingosine-induced apoptosis is dependent on lysosomal proteases. Biochem J 2001; 359:335-43; PMID: 11583579; http://dx.doi.org/10.1042/0264-6021: 3590335
18. Heinrich M, Wickel M, Schneider-Brachert W, Sandberg C, Gahr J, Schwandner R, et al. Cathepsin D targeted by acid sphingomyelinase-derived ceramide. EMBO J 1999; 18:5252-63; PMID:10508159; http:// dx.doi.org/10.1093/ emboj/18.19.5252
19. Larrick JW, Cresswell P. Modulation of cell surface iron transferrin receptors by cellular density and state of activation. J Supramol Struct 1979; 11:579-86; PMID: 232525; http://dx.doi.org/10.1002/jss.400110415
20. Renau-Piqueras J, Miragall F, Cervera J. Endocytosis of cationized ferritin in human peripheral blood by resting T-lymphocytes. Cell Tissue Res 1985; 240: 743-6; PMID:3874694; http://dx.doi.org/10.1007/ BF00216363
21. Kakudo T, Chaki S, Futaki S, Nakase I, Akaji K, Kawakami T, et al. Transferrin-modified liposomes equipped with a pH-sensitive fusogenic peptide: an artificial viral-like delivery system. Biochemistry 2004; 43:5618-28; PMID:15134436; http://dx.doi.org/10. 1021/bi035802w
22. Li X, Ding L, Xu Y, Wang Y, Ping Q. Targeted delivery of doxorubicin using stealth liposomes modified with transferrin. Int J Pharm 2009; 373:116-23; PMID: 19429296; http://dx.doi.org/10.1016/j.ijpharm.2009. 01.023
23. Kobayashi T, Ishida T, Okada Y, Ise S, Harashima H, Kiwada H. Effect of transferrin receptor-targeted liposomal doxorubicin in P-glycoprotein-mediated drug resistant tumor cells. Int J Pharm 2007; 329:94-102; PMID:16997518; http://dx.doi.org/10.1016/j.ijpharm. 2006.08.039
24. Hong M, Zhu S, Jiang Y, Tang G, Pei Y. Efficient tumor targeting of hydroxycamptothecin loaded PEGylated niosomes modified with transferrin. J Control Release 2009; 133:96-102; PMID:18840485; http://dx.doi.org/10.1016/j. jconrel.2008.09.005
25. Heuser J, Kirchhausen T. Deep-etch views of clathrin assemblies. J Ultrastruct Res 1985; 92:1-27; PMID: 2870198; http://dx.doi.org/10.1016/0889- 1605(85) 90123-5
26. Enoch HG, Strittmatter P. Formation and properties of 1000-A-diameter, single-bilayer phospholipid vesicles. Proc Natl Acad Sci USA 1979; 76:145-9; PMID: 34148; http://dx.doi.org/10.1073/pnas.76.1.145
27. Ishida T, Iden DL, Allen TM. A combinatorial approach to producing sterically stabilized (Stealth) immunoliposomal drugs. FEBS Lett 1999; 460:129-33; PMID:10571074; http://dx.doi.org/10.1016/S0014- 5793(99)01320-4
28. McIntyre JC, Sleight RG. Fluorescence assay for phospholipid membrane asymmetry. Biochemistry 1991; 30:11819-27; PMID:1751498; http://dx.doi.org/10. 1021/bi00115a012
29. Olsson GM, Rungby J, Rundquist I, Brunk UT. Evaluation of lysosomal stability in living cultured macrophages by cytofluorometry. Effect of silver lactate and hypotonic conditions. Virchows Arch B Cell Pathol Incl Mol Pathol 1989; 56:263-9; PMID:2565621; http://dx.doi.org/10.1007/BF02890025
30. Khazanov E, Priev A, Shillemans JP, Barenholz Y. Physicochemical and biological characterization of ceramide-containing liposomes: paving the way to ceramide therapeutic application. Langmuir 2008; 24:6965-80; PMID:18512883; http://dx.doi.org/10. 1021/la800207z
31. Shabbits JA, Mayer LD. Intracellular delivery of ceramide lipids via liposomes enhances apoptosis in vitro. Biochim Biophys Acta 2003; 1612:98-106; PMID:12729935; http://dx.doi.org/10.1016/S0005- 2736(03)00108-1
32. Radin NS. Killing cancer cells by poly-drug elevation of ceramide levels: a hypothesis whose time has come? Eur J Biochem 2001; 268:193-204; PMID:11168352; http://dx.doi.org/10.1046/j.1432-1033.2001.01845.x
33. Stover T, Kester M. Liposomal delivery enhances shortchain ceramide-induced apoptosis of breast cancer cells. J Pharmacol Exp Ther 2003; 307:468-75; PMID: 12975495; http://dx.doi.org/10.1124/jpet.103.054056
34. Stover TC, Sharma A, Robertson GP, Kester M. Systemic delivery of liposomal short-chain ceramide limits solid tumor growth in murine models of breast adenocarcinoma. Clin Cancer Res 2005; 11:3465-74; PMID:15867249; http://dx.doi.org/10.1158/1078-0432.CCR-04-1770
35. Siskind LJ, Colombini M. The lipids C2- and C16- ceramide form large stable channels. Implications for apoptosis. J Biol Chem 2000; 275:38640-4; PMID: 11027675; http://dx.doi.org/10.1074/jbc.C000587200
36. Boddapati SV, D'Souza GG, Erdogan S, Torchilin VP, Weissig V. Organelle-targeted nanocarriers: specific delivery of liposomal ceramide to mitochondria enhances its cytotoxicity in vitro and in vivo. Nano Lett 2008; 8:2559-63; PMID:18611058; http://dx.doi. org/10.1021/nl801908y
37. Vermes I, Haanen C, Steffens-Nakken H, Reutelingsperger C. A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V. J Immunol Methods 1995; 184:39-51; PMID:7622868; http://dx.doi.org/10.1016/0022-1759(95)00072-I
38. Zdolsek J, Zhang H, Roberg K, Brunk U. H2O2- mediated damage to lysosomal membranes of J-774 cells. Free Radic Res Commun 1993; 18:71-85; PMID: 8386686;http://dx.doi.org/10.3109/10715769309147344