From serendipity to mitochondria-targeted nanocarriers

Pharmaceutical Research

Volumn 28, Issue 11, 2011, Pages 2657-2668

  Weissig, Volkmar ^a  

^a MIDWESTERN UNIVERSITY   (United States)

Author keywords

Apoptosis; Dequalinium; DQAsomes; Gene therapy; Mitochondria; Mitochondria specific liposomes; Mitochondria targeted nanocarriers; STPP liposomes; Triphenylphosphonium

Indexed keywords

CHEMICAL COMPOUND; DEQUALINIUM BASED LIPOSOME; DRUG CARRIER; ETOPOSIDE; LIPOSOME; LOW MOLECULAR WEIGHT COMPOUND; MITOCHONDRIAL DNA; NANOCARRIER; PACLITAXEL; STEARYL TRIPHENYLPHOSPHONIUM BROMIDE LIPOSOME; UNCLASSIFIED DRUG;

CANCER CELL DESTRUCTION; COLON CARCINOMA; DRUG ACCUMULATION; DRUG DELIVERY SYSTEM; DRUG DOSAGE FORM COMPARISON; DRUG MECHANISM; DRUG STRUCTURE; DRUG TARGETING; GENE TARGETING; HUMAN; LIPOSOMAL DELIVERY; LIPOSOMAL GENE DELIVERY SYSTEM; MITOCHONDRIAL TARGETING; MOLECULAR WEIGHT; NANOTECHNOLOGY; NONHUMAN; PRIORITY JOURNAL; REVIEW; TARGET CELL;

DNA; DRUG CARRIERS; DRUG DELIVERY SYSTEMS; HUMANS; MITOCHONDRIA; MOLECULAR TARGETED THERAPY; NANOSTRUCTURES; PHARMACEUTICAL PREPARATIONS;

EID: 84855601316     PISSN: 07248741     EISSN: 1573904X     Source Type: Journal    
DOI: 10.1007/s11095-011-0556-9     Document Type: Review

References (118)

1. Mobacken H, Romanus M. Microvascular response to local application of dequalinium chloride. A vital microscopical study of hamster's cheek pouch and a microangiographic study of rabbit's ear. Br J Dermatol. 1975;92(1):63-72.
2. Mobacken H, Romanus M, Wengstrom C. Development of strength in dequalinium chloride-treated skin incisions in rat. Dermatologica. 1974;148(3):154-9.
3. Weiss MJ, Wong JR, Ha CS, Bleday R, Salem RR, Steele Jr GD, et al. Dequalinium, a topical antimicrobial agent, displays anticarcinoma activity based on selective mitochondrial accumulation. Proc Natl Acad Sci USA. 1987;84 (15):5444-8. (Pubitemid 17129017)
4. Christman JE, Miller DS, Coward P, Smith LH, Teng NN. Study of the selective cytotoxic properties of cationic, lipophilic mitochondrial-specific compounds in gynecologic malignancies. Gynecol Oncol. 1990;39(1):72-9. (Pubitemid 20378263)
5. Steichen JD, Weiss MJ, Elmaleh DR, Martuza RL. Enhanced in vitro uptake and retention of 3H-tetraphenylphosphonium by nervous system tumor cells. J Neurosurg. 1991;74(1):116-22.
6. Vercesi AE, Bernardes CF, Hoffmann ME, Gadelha FR, Docampo R. Digitonin permeabilization does not affect mitochondrial function and allows the determination of the mitochondrial membrane potential of Trypanosoma cruzi in situ. J Biol Chem. 1991;266(22):14431-4. (Pubitemid 21907520)
7. Horobin RW, Trapp S, Weissig V. Mitochondriotropics: a review of their mode of action, and their applications for drug and DNA delivery to mammalian mitochondria. J Control Release. 2007;121(3):125-36. (Pubitemid 47212544)
8. Galanakis D, Davis CA, Del Rey Herrero B, Ganellin CR, Dunn PM, Jenkinson DH. Synthesis and structure-activity relationships of dequalinium analogues as K+ channel blockers. Investigations on the role of the charged heterocycle. J Med Chem. 1995;38 (4):595-606.
9. Zhuo S, Allison WS. Inhibition and photoinactivation of the bovine heart mitochondrial F1-ATPase by the cytotoxic agent, dequalinium. Biochem Biophys Res Commun. 1988;152(3): 968-72.
10. Hait WN. Targeting calmodulin for the development of novel cancer chemotherapeutic agents. Anticancer Drug Des. 1987;2:139-49. (Pubitemid 18043260)
11. Dong Y, Berners-Price SJ, Thorburn DR, Antalis T, Dickinson J, Hurst T, et al. Serine protease inhibition and mitochondrial dysfunction associated with cisplatin resistance in human tumor cell lines: targets for therapy. Biochem Pharmacol. 1997;53 (11):1673-82. (Pubitemid 27356097)
12. Manetta A, Emma D, Gamboa G, Liao S, Berman M, DiSaia P. Failure to enhance the in vivo killing of human ovarian carcinoma by sequential treatment with dequalinium chloride and tumor necrosis factor. Gynecol Oncol. 1993;50 (1):38-44. (Pubitemid 23235509)
13. Bleday R, Weiss MJ, Salem RR, Wilson RE, Chen LB, Steele Jr G. Inhibition of rat colon tumor isograft growth with dequalinium chloride. Arch Surg. 1986;121(11):1272-5.
14. Schneider Berlin KR, Ammini CV, Rowe TC. Dequalinium induces a selective depletion of mitochondrial DNA from HeLa human cervical carcinoma cells. Exp Cell Res. 1998;245(1):137-45. (Pubitemid 28551063)
15. Schneider-Berlin KR, Bonilla TD, Rowe TC. Induction of petite mutants in yeast Saccharomyces cerevisiae by the anticancer drug dequalinium. Mutat Res. 2005;572(1-2):84-97. (Pubitemid 40403656)
16. Sancho P, Galeano E, Nieto E, Delgado MD, Garcia-Perez AI. Dequalinium induces cell death in human leukemia cells by early mitochondrial alterations which enhance ROS production. Leuk Res. 2007;31(7):969-78. (Pubitemid 46856728)
17. Rodrigues JR, Gamboa ND. Effect of dequalinium on the oxidative stress in Plasmodium berghei-infected erythrocytes. Parasitol Res. 2009;104(6):1491-6.
18. Gamboa-Vujicic G, Emma DA, Liao SY, Fuchtner C, Manetta A. Toxicity of the mitochondrial poison dequalinium chloride in a murine model system. J Pharm Sci. 1993;82(3):231-5. (Pubitemid 23150399)
19. Armijo Moreno M, Gutierrez Salmeron MT, Camacho Martinez F, Naranjo Sintes R, Armijo Lozano R, Garcia Mellado V, et al. Necrosis of the penis caused by dequalinim (2 findings). Actas Dermosifiliogr. 1976;67(7-8):547-52.
20. Weissig V, Vetro-Widenhouse TS, Rowe TC. Topoisomerase II inhibitors induce cleavage of nuclear and 35-kb plastid DNAs in the malarial parasite Plasmodium falciparum. DNA Cell Biol. 1997;16(12):1483-92. (Pubitemid 28070528)
21. Khor V, Yowell C, Dame JB, Rowe TC. Expression and characterization of the ATP-binding domain of a malarial Plasmodium vivax gene homologous to the B-subunit of the bacterial topoisomerase DNA gyrase. Mol Biochem Parasitol. 2005;140(1):107-17. (Pubitemid 40203420)
22. Rowe TC, Weissig V, Lawrence JW. Mitochondrial DNA metabolism targeting drugs. Adv Drug Deliv Rev. 2001; 49(1-2):175-87. (Pubitemid 32493807)
23. Weissig V, Lasch J, Erdos G, Meyer HW, Rowe TC, Hughes J. DQAsomes: a novel potential drug and gene delivery system made from Dequalinium. Pharm Res. 1998;15(2):334-7. (Pubitemid 28144249)
24. Gulik A, Luzzati V, DeRosa M, Gambacorta A. Tetraether lipid components from a thermoacidophilic archaebacterium. Chemical structure and physical polymorphism. J Mol Biol. 1988;201 (2):429-35.
25. Luzzati V, Gambacorta A, DeRosa M, Gulik A. Polar lipids of thermophilic prokaryotic organisms: chemical and physical structure. Annu Rev Biophys Biophys Chem. 1987;16: 25-47.
26. De Rosa M, Gambacorta A, Gliozzi A. Structure, biosynthesis, and physicochemical properties of archaebacterial lipids. Microbiol Rev. 1986;50(1):70-80. (Pubitemid 16122596)
27. Weissig V, Torchilin VP. Mitochondriotropic cationic vesicles: a strategy towards mitochondrial gene therapy. Curr Pharm Biotechnol. 2000;1(4):325-46.
28. Weissig V, Moegel H-J, Wahab M, Lasch J. Computer simulation of DQAsomes. Proc Intl Symp Control Rel Bioact Mater. 1998;25:196-7.
29. Grinberg S, Kolot V, Linder C, Shaubi E, Kas'yanov V, Deckelbaum RJ, et al. Synthesis of novel cationic bolaamphiphiles from vernonia oil and their aggregated structures. Chem Phys Lipids. 2008;153(2):85-97.
30. Li Q, Mittal R, Huang L, Travis B, Sanders CR. Bolaamphiphileclass surfactants can stabilize and support the function of solubilized integral membrane proteins. Biochemistry. 2009;48(49):11606-8.
31. Meister A, Drescher S, Garamus VM, Karlsson G, Graf G, Dobner B, et al. Temperature-dependent self-assembly and mixing behavior of symmetrical single-chain bolaamphiphiles. Langmuir. 2008;24(12):6238-46.
32. Meister A, Weygand MJ, Brezesinski G, Kerth A, Drescher S, Dobner B, et al. Evidence for a reverse U-shaped conformation of single-chain bolaamphiphiles at the air-water interface. Langmuir. 2007;23(11):6063-9. (Pubitemid 46868674)
33. Puri A, Loomis K, Smith B, Lee JH, Yavlovich A, Heldman E, et al. Lipid-based nanoparticles as pharmaceutical drug carriers: from concepts to clinic. Crit Rev Ther Drug Carrier Syst. 2009;26(6):523-80.
34. Qiu F, Chen Y, Tang C, Zhou Q, Wang C, Shi YK, et al. De novo design of a bolaamphiphilic peptide with only natural amino acids. Macromol Biosci. 2008;8(11):1053-9.
35. Fuchtner C, Emma DA, Manetta A, Gamboa G, Bernstein R, Liao SY. Characterization of a human ovarian carcinoma cell line: UCI 101. Gynecol Oncol. 1993;48(2):203-9. (Pubitemid 23075173)
36. Weissig V, Lizano C, Ganellin CR, Torchilin VP. DNA binding cationic bolasomes with delocalized charge center: a structureactivity relationship study. STP Pharma Sci. 2001;11:91-6. (Pubitemid 32154864)
37. Felgner PL, Gadek TR, Holm M, Roman R, Chan HW, Wenz M, et al. Lipofection: a highly efficient, lipid-mediated DNAtransfection procedure. Proc Natl Acad Sci USA. 1987;84 (21):7413-7.
38. TrosdeIlarduya C, Sun Y, Duzgunes N. Gene delivery by lipoplexes and polyplexes. Eur J Pharm Sci. 2010;40(3):159-70.
39. Hart SL. Multifunctional nanocomplexes for gene transfer and gene therapy. Cell Biol Toxicol. 2010;26(1):69-81.
40. He CX, Tabata Y, Gao JQ. Non-viral gene delivery carrier and its three-dimensional transfection system. Int J Pharm. 2010;386 (1-2):232-42.
41. Montier T, Benvegnu T, Jaffres PA, Yaouanc JJ, Lehn P. Progress in cationic lipid-mediated gene transfection: a series of bio-inspired lipids as an example. Curr Gene Ther. 2008;8 (5):296-312.
42. Ma B, Zhang S, Jiang H, Zhao B, Lv H. Lipoplex morphologies and their influences on transfection efficiency in gene delivery. J Control Release. 2007;123(3):184-94. (Pubitemid 350007826)
43. Duguid JG, Durland RH. DNA packaging in non-viral systems. In: Rolland A, editor. Advanced gene delivery. Amsterdam: Harwood Academic; 1999. p. 45-63.
44. Sternberg B, Sorgi FL, Huang L. New structures in complex formation between DNA and cationic liposomes visualized by freeze-fracture electron microscopy. FEBS Lett. 1994;356 (2-3):361-6. (Pubitemid 24377008)
45. Lasch J, Meye A, Taubert H, Koelsch R, Mansa-ard J, Weissig V. Dequalinium vesicles form stable complexes with plasmid DNA which are protected from DNase attack. Biol Chem. 1999;380(6):647-52. (Pubitemid 29322354)
46. Xu Y, Szoka Jr FC. Mechanism of DNA release from cationic liposome/DNA complexes used in cell transfection. Biochemistry. 1996;35(18):5616-23. (Pubitemid 26143656)
47. Weissig V, Torchilin VP. Towards mitochondrial gene therapy: DQAsomes as a strategy. J Drug Target. 2001;9(1):1-13. (Pubitemid 32496446)
48. Weissig V, D'Souza GGM. Cationic mitochondriotropic vesicles for DNA delivery to mitochondria. Mol Ther. 2004;9:S259.
49. Therapy ASfG. KEYWORD INDEX. Molecular Therapy 2004;9:S425-35.
50. Wallace DC, Singh G, Lott MT, Hodge JA, Schurr TG, Lezza AM, et al. Mitochondrial DNA mutation associated with Leber's hereditary optic neuropathy. Science. 1988;242 (4884):1427-30. (Pubitemid 19008070)
51. Holt IJ, Harding AE, Morgan-Hughes JA. Deletions of muscle mitochondrial DNA in patients with mitochondrial myopathies. Nature. 1988;331(6158):717-9. (Pubitemid 18062238)
52. TuppenHA, Blakely EL, TurnbullDM, Taylor RW.Mitochondrial DNA mutations and human disease. Biochim Biophys Acta. 2010;1797(2):113-28.
53. Naviaux RK. Developing a systematic approach to the diagnosis and classification of mitochondrial disease. Mitochondrion. 2004;4(5-6):351-61. (Pubitemid 39646789)
54. Claros MG, Perea J, Jacq C. Allotopic expression of yeast mitochondrial maturase to study mitochondrial import of hydrophobic proteins. Methods Enzymol. 1996;264:389-403.
55. Gray RE, Law RH, Devenish RJ, Nagley P. Allotopic expression of mitochondrial ATP synthase genes in nucleus of Saccharomyces cerevisiae. Methods Enzymol. 1996;264:369-89.
56. Weissig V, Torchilin VP. Cationic bolasomes with delocalized charge centers as mitochondria-specific DNA delivery systems. Adv Drug Deliv Rev. 2001;49(1-2):127-49. (Pubitemid 32493805)
57. Zullo SJ, Parks WT, Chloupkova M, Wei B, Weiner H, Fenton WA, et al. Stable transformation of CHO Cells and human NARP cybrids confers oligomycin resistance (oli(r)) following transfer of a mitochondrial DNA-encoded oli(r) ATPase6 gene to the nuclear genome: a model system for mtDNA gene therapy. Rejuvenation Res. 2005;8(1):18-28.
58. Manfredi G, Fu J, Ojaimi J, Sadlock JE, Kwong JQ, Guy J, et al. Rescue of a deficiency in ATP synthesis by transfer of MTATP6, a mitochondrial DNA-encoded gene, to the nucleus. Nat Genet. 2002;30(4):394-9.
59. Oca-Cossio J, Kenyon L, Hao H, Moraes CT. Limitations of allotopic expression of mitochondrial genes in mammalian cells. Genetics. 2003;165(2):707-20. (Pubitemid 37337637)
60. de Grey AD. Mitochondrial gene therapy: an arena for the biomedical use of inteins. Trends Biotechnol. 2000;18(9):394-9.
61. Figueroa-Martinez F, Vazquez-Acevedo M, Cortes-Hernandez P, Garcia-Trejo JJ, Davidson E, King MP, et al. What limits the allotopic expression of nucleus-encoded mitochondrial genes? The case of the chimeric Cox3 and Atp6 genes. Mitochondrion. 2011;11(1):147-54.
62. Perales-Clemente E, Fernandez-Silva P, Acin-Perez R, Perez- Martos A, Enriquez JA. Allotopic expression of mitochondrialencoded genes in mammals: achieved goal, undemonstrated mechanism or impossible task? Nucleic Acids Res. 2011;39 (1):225-34.
63. Yoon YG, Yang YW, Koob MD. PCR-based cloning of the complete mouse mitochondrial genome and stable engineering in Escherichia coli. Biotechnol Lett. 2009;31(11):1671-6.
64. Yonemura I, Nakada K, Sato A, Hayashi J, Fujita K, Kaneko S, et al. Direct cloning of full-length mouse mitochondrial DNA using a Bacillus subtilis genome vector. Gene. 2007;391(1-2):171-7. (Pubitemid 46357665)
65. Bigger B, Tolmachov O, Collombet JM, Coutelle C. Introduction of chloramphenicol resistance into the modified mouse mitochondrial genome: cloning of unstable sequences by passage through yeast. Anal Biochem. 2000;277(2):236-42. (Pubitemid 30055873)
66. Bigger BW, Coutelle C. Trial and error: how the unclonable human mitochondrial genome was cloned in yeast. Pharm Res. 2011;IN PRESS.
67. Gibson DG, Glass JI, Lartigue C, Noskov VN, Chuang RY, Algire MA, et al. Creation of a bacterial cell controlled by a chemically synthesized genome. Science. 2010;329(5987):52-6.
68. Koulintchenko M, Temperley RJ, Mason PA, Dietrich A, Lightowlers RN. Natural competence of mammalian mitochondria allows the molecular investigation of mitochondrial gene expression. Hum Mol Genet. 2006;15(1):143-54. (Pubitemid 43020112)
69. Weissig V, Seibel P, Seibel M, Torchilin VP. Binding and release of DNA-peptide conjugates by cationic mitochondriotropic vesicles (DQAsomes). Proc Intl Symp Control Rel Bioact Mater. 2001;28:850-1.
70. Weissig V, Lizano C, Torchilin VP. Selective DNA release from DQAsome/DNA complexes at mitochondria-like membranes. Drug Deliv. 2000;7(1):1-5. (Pubitemid 30118345)
71. Weissig V, D'Souza GG, Torchilin VP. DQAsome/DNA complexes release DNA upon contact with isolated mouse liver mitochondria. J Control Release. 2001;75(3):401-8. (Pubitemid 32727269)
72. D'Souza GG, Rammohan R, Cheng SM, Torchilin VP, Weissig V. DQAsome-mediated delivery of plasmid DNA toward mitochondria in living cells. J Control Release. 2003;92 (1-2):189-97. (Pubitemid 37138687)
73. Katrangi E, D'Souza G, Boddapati SV, Kulawiec M, Singh KK, Bigger B, et al. Xenogenic transfer of isolated murine mitochondria into human rho0 cells can improve respiratory function. Rejuvenation Res. 2007;10(4):561-70.
74. Vaidya B, Mishra N, Dube D, Tiwari S, Vyas SP. Targeted nucleic acid delivery to mitochondria. Curr Gene Ther. 2009;9 (6):475-86.
75. Yoon YG, Koob MD, Yoo YH. Re-engineering the mitochondrial genomes in mammalian cells. Anat Cell Biol. 2010;43 (2):97-109.
76. Lyrawati D, Trounson A, Cram D. Expression of GFP in the mitochondrial compartment using DQAsome-mediated delivery of an artificial mini-mitochondrial genome. Pharm Res. 2011;IN PRESS.
77. Lechardeur D, Lukacs GL. Intracellular barriers to non-viral gene transfer. Curr Gene Ther. 2002;2(2):183-94.
78. Duvvuri M, Feng W, Mathis A, Krise JP. A cell fractionation approach for the quantitative analysis of subcellular drug disposition. Pharm Res. 2004;21(1):26-32. (Pubitemid 38122288)
79. Duvvuri M, Gong Y, Chatterji D, Krise JP. Weak base permeability characteristics influence the intracellular sequestration site in the multidrug-resistant human leukemic cell line HL-60. J Biol Chem. 2004;279(31):32367-72. (Pubitemid 39014690)
80. Horobin RW. Uptake, distribution and accumulation of dyes and fluorescent probes within living cells: a structure-activity modelling approach. Adv Colour Sci Technol. 2001;4:101-7.
81. Green DR, Reed JC. Mitochondria and apoptosis. Science. 1998;281(5381):1309-12. (Pubitemid 28406816)
82. Skulachev VP. Why are mitochondria involved in apoptosis? Permeability transition pores and apoptosis as selective mechanisms to eliminate superoxide-producing mitochondria and cell. FEBS Lett. 1996;397(1):7-10. (Pubitemid 26380163)
83. Chen G, Wang F, Trachootham D, Huang P. Preferential killing of cancer cells with mitochondrial dysfunction by natural compounds. Mitochondrion. 2010;10(6):614-25.
84. Biasutto L, Dong LF, Zoratti M, Neuzil J. Mitochondrially targeted anti-cancer agents. Mitochondrion. 2010;10(6): 670-81.
85. Ralph SJ, Rodriguez-Enriquez S, Neuzil J, Moreno-Sanchez R. Bioenergetic pathways in tumor mitochondria as targets for cancer therapy and the importance of the ROS-induced apoptotic trigger. Mol Aspects Med. 2010;31(1):29-59.
86. Guchelaar HJ, Vermes A, Vermes I, Haanen C. Apoptosis: molecular mechanisms and implications for cancer chemotherapy. Pharm World Sci. 1997;19(3):119-25. (Pubitemid 27334513)
87. Decaudin D, Marzo I, Brenner C, Kroemer G. Mitochondria in chemotherapy-induced apoptosis: a prospective novel target of cancer therapy (review). Int J Oncol. 1998;12(1):141-52. (Pubitemid 28027240)
88. Andre N, Braguer D, Brasseur G, Goncalves A, Lemesle-Meunier D, Guise S, et al. Paclitaxel induces release of cytochrome c from mitochondria isolated from human neuroblastoma cells'. Cancer Res. 2000;60(19):5349-53.
89. Cheng SM, Pabba S, Torchilin VP, Fowle W, Kimpfler A, Schubert, et al. Towards mitochondria-specific delivery of apoptosis-inducing agents: DQAsomal incorporated paclitaxel. J Drug Del Sci Tech. 2005;15(1):81-6. (Pubitemid 40208983)
90. D'Souza GG, Cheng SM, Boddapati SV, Horobin RW, Weissig V. Nanocarrier-assisted sub-cellular targeting to the site of mitochondria improves the pro-apoptotic activity of paclitaxel. J Drug Target. 2008;16(7):578-85.
91. Vaidya B, Paliwal R, Rai S, Khatri K, Goyal AK, Mishra N, et al. Cell-selective mitochondrial targeting: a new approach for cancer therapy. Cancer Ther. 2009;7:141-8.
92. Zhang Y, Li RJ, Ying X, Tian W, Yao HJ, Men Y, et al. Targeting therapy with mitosomal daunorubicin plus amlodipine has the potential to circumvent intrinsic resistant breast cancer. Mol Pharm. 2011;8(1):162-75.
93. Weissig V, Lizano C, Torchilin VP. Micellar delivery system for dequalinium-A lipophilic cationic drug with anticarcinoma activity. J Liposome Res. 1998;8:391-400. (Pubitemid 28462817)
94. Murphy MP, Smith RA. Drug delivery to mitochondria: the key to mitochondrial medicine. Adv Drug Deliv Rev. 2000;41 (2):235-50. (Pubitemid 30122962)
95. Smith RA, Porteous CM, Coulter CV, Murphy MP. Selective targeting of an antioxidant to mitochondria. Eur J Biochem. 1999;263(3):709-16. (Pubitemid 29361943)
96. Boddapati SV, Tongcharoensirikul P, Hanson RN, D'Souza GG, Torchilin VP, Weissig V. Mitochondriotropic liposomes. J Liposome Res. 2005;15(1-2):49-58. (Pubitemid 40976306)
97. Schmidt MF. Fatty acid binding: a new kind of posttranslational modification of membrane proteins. Curr Top Microbiol Immunol. 1983;102:101-29.
98. Magee AI, Schlesinger MJ. Fatty acid acylation of eucaryotic cell membrane proteins. Biochim Biophys Acta. 1982;694 (3):279-89. (Pubitemid 13177352)
99. Schlesinger MJ, Magee AI. Fatty Acid acylation of membrane proteins. Biophys J. 1982;37(1):126-7.
100. Weissig V, Lasch J, Klibanov AL, Torchilin VP. A new hydrophobic anchor for the attachment of proteins to liposomal membranes. FEBS Lett. 1986;202(1):86-90. (Pubitemid 16051133)
101. Weissig V, Lasch J, Gregoriadis G. Covalent coupling of sugars to liposomes. Biochim Biophys Acta. 1989;1003(1):54-7. (Pubitemid 19124008)
102. Weissig V, Gregoriadis G. Coupling of aminogroup bearing ligands to liposomes. In: Gregoriadis G, editor. Liposome technology. Boca Raton: CRC; 1992. p. 231-48.
103. Torchilin VP, Weissig V, Martin FJ, Heath TD, News RRC. Surface modification of liposomes. In: Torchilin VP, Weissig V, editors. Liposomes-A practical approach. 2nd ed. Oxford: Oxford University Press; 2003. p. 193-229.
104. 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(8):2559-63.
105. Martin B, Sainlos M, Aissaoui A, Oudrhiri N, Hauchecorne M, Vigneron JP, et al. The design of cationic lipids for gene delivery. Curr Pharm Des. 2005;11(3):375-94. (Pubitemid 40277864)
106. Nicolazzi C, Garinot M, Mignet N, Scherman D, Bessodes M. Cationic lipids for transfection. Curr Med Chem. 2003;10 (14):1263-77. (Pubitemid 36763934)
107. Hirko A, Tang F, Hughes JA. Cationic lipid vectors for plasmid DNA delivery. Curr Med Chem. 2003;10(14):1185-93. (Pubitemid 36763929)
108. Schatzlein AG. Non-viral vectors in cancer gene therapy: principles and progress. Anticancer Drugs. 2001;12(4):275-304. (Pubitemid 32453434)
109. Kim CK, Haider KH, Lim SJ. Gene medicine: a new field of molecular medicine. Arch Pharm Res. 2001;24(1):1-15.
110. Siskind LJ, Colombini M. The lipids C2- and C16-ceramide form large stable channels. Implications for apoptosis. J Biol Chem. 2000;275(49):38640-4. (Pubitemid 32009194)
111. Siskind LJ. Mitochondrial ceramide and the induction of apoptosis. J Bioenerg Biomembr. 2005;37(3):143-53. (Pubitemid 41420469)
112. Siskind LJ, Feinstein L, Yu T, Davis JS, Jones D, Choi J, et al. Anti-apoptotic Bcl-2 family proteins disassemble ceramide channels. J Biol Chem. 2008;283(11):6622-30.
113. 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(9):3465-74. (Pubitemid 40627901)
114. Patel NR, Hatziantoniou S, Georgopoulos A, Demetzos C, Torchilin VP, Weissig V, et al. Mitochondria-targeted liposomes improve the apoptotic and cytotoxic action of sclareol. J Liposome Res. 2010;20(3):244-9.
115. Dimas K, Hatziantoniou S, Tseleni S, Khan H, Georgopoulos A, Alevizopoulos K, et al. Sclareol induces apoptosis in human HCT116 colon cancer cells in vitro and suppression of HCT116 tumor growth in immunodeficient mice. Apoptosis. 2007;12 (4):685-94. (Pubitemid 46411476)
116. Dimas K, Demetzos C, Vaos V, Ioannidis P, Trangas T. Labdane type diterpenes down-regulate the expression of c-Myc protein, but not of Bcl-2, in human leukemia T-cells undergoing apoptosis. Leuk Res. 2001;25(6):449-54. (Pubitemid 32401561)
117. Dimas K, Kokkinopoulos D, Demetzos C, Vaos B, Marselos M, Malamas M, et al. The effect of sclareol on growth and cell cycle progression of human leukemic cell lines. Leuk Res. 1999;23 (3):217-34. (Pubitemid 29083377)
118. Paradissis A, Hatziantoniou S, Georgopoulos A, Psarra AM, Dimas K, Demetzos C. Liposomes modify the subcellular distribution of sclareol uptake by HCT-116 cancer cell lines. Biomed Pharmacother. 2007;61(2-3):120-4. (Pubitemid 46578283)