Multiple triphenylphosphonium cations as a platform for the delivery of a pro-apoptotic peptide

Pharmaceutical Research

Volumn 28, Issue 11, 2011, Pages 2780-2789

  Kolevzon, Netanel ^a   Kuflik, Uriel ^a   Shmuel, Miriam ^a   Benhamron, Sandrine ^a   Ringel, Israel ^a   Yavin, Eylon ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Antimicrobial peptide; Apoptosis; Mitochondria; Tripenylphosphonium

Indexed keywords

CATION; CYTOTOXIC FACTOR; DEXTRO LYSYLLEUCYLALANYLLYSYLLEUCYLALANYLLYSYLLYSYLLEUCYLALANYLLYSYLLEUCYLALANYLLYSINE; FLUORESCEIN ISOTHIOCYANATE; LIPOCORTIN 5; LYSINE; TRIPHENYLPHOSPHONIUM CATION; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; APOPTOSIS; ARTICLE; CANCER CELL DESTRUCTION; CELL TRANSFER; CELL VIABILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOTOXICITY TEST; DRUG DELIVERY SYSTEM; DRUG MECHANISM; FLUORESCENCE ACTIVATED CELL SORTING; HELA CELL; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LIPOPROTEIN METABOLISM; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN TRANSPORT;

ANNEXIN A5; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CATIONS; CELL CULTURE TECHNIQUES; DRUG COMPOUNDING; DRUG DELIVERY SYSTEMS; FLUORESCEIN-5-ISOTHIOCYANATE; FLUORESCENT DYES; HELA CELLS; HUMANS; MITOCHONDRIA; MOLECULAR TARGETED THERAPY; ORGANOPHOSPHORUS COMPOUNDS; PEPTIDES; PROPIDIUM;

EID: 84856217682     PISSN: 07248741     EISSN: 1573904X     Source Type: Journal    
DOI: 10.1007/s11095-011-0494-6     Document Type: Article

References (61)

1. Ross MF, Prime TA, Abakumova I, James AM, Porteous CM, Smith RAJ, et al. Rapid and extensive uptake and activation of hydrophobic triphenylphosphonium cations within cells. Biochem J. 2008;411:633-45. (Pubitemid 351600748)
2. Filipovska A, Kelso GF, Brown SE, Beer SM, Smith RAJ, Murphy MP. Synthesis and characterization of a triphenylphosphoniumconjugated peroxidase mimetic. J Biol Chem. 2005;280:24113-26.
3. Seibel P, Trappe J, Villani G, Klopstock T, Papa S, Reichmann H. Transfection of mitochondria: strategy towards a gene therapy of mitochondrial DNA diseases. Nucl Acids Res. 1995;23:10-7.
4. Pathania D, Millard M, Neamati N. Opportunities in discovery and delivery of anticancer drugs targeting mitochondria and cancer cell metabolism. Adv Drug Del Rev. 2009;61:1250-75.
5. Weissig V, Cheng S-M, D'Souza GGM. Mitochondrial pharmaceutics. Mitochondrion. 2004;3:229-44. (Pubitemid 38263637)
6. Mukhopadhyay A, Weiner H. Delivery of drugs and macromolecules to mitochondria. Adv Drug Del Rev. 2007;59:729-38. (Pubitemid 47320812)
7. Hoye AT, Davoren JE, Wipf P, Fink MP, Kagan VE. Targeting Mitochondria. Acc Chem Res. 2008;41:87-97.
8. Torchilin VP. Recent approaches to intracellular delivery of drugs and DNA and organelle targeting. AnnuRev Biomed Eng. 2006;8:343-75. (Pubitemid 44314821)
9. Yamada Y, Akita H, Kogure K, Kamiya H, Harashima H. Mitochondrial drug delivery and mitochondrial disease therapy - an approach to liposome-based delivery targeted to mitochondria. Mitochondrion. 2007;7:63-71. (Pubitemid 46351977)
10. PatelNR,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;20:244-9.
11. Yasuzaki Y, Yamada Y, Harashima H. Mitochondrial matrix delivery using MITO-Porter, a liposome-based carrier that specifies fusion with mitochondrial membranes. Biochem Biophys Res Comm. 2010;397:181-6.
12. Weissig V, Boddapati SV, Cheng S-M, D'Souza GGM. Liposomes and liposome-like vesicles for drug and DNA delivery to mitochondria. J Liposome Res. 2006;16:249-64. (Pubitemid 44358998)
13. Yamada Y, Akita H, Kamiya H, Kogure K, Yamamoto T, Shinohara Y, et al. MITO-Porter: a liposome-based carrier system for delivery of macromolecules into mitochondria via membrane fusion. Biochim Biophys Acta. 2008;1778:423-32.
14. D'Souza GGM, Cheng S-M, 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;16:578-85.
15. Hickey JL, Ruhayel RA, Barnard PJ, Baker MV, Berners-Price SJ, Filipovska A. Mitochondria-targeted chemotherapeutics: the rational design of Gold(I) N-heterocyclic carbene complexes that are selectively toxic to cancer cells and target protein selenols in preference to thiols. J Am Chem Soc. 2008;130:12570-1.
16. Ke H, Wang H, Wong W-K, Mak N-K, Kwong DWJ, Wong K-L, et al. Responsive and mitochondria-specific ruthenium(II) in-vitro applications: two-photon (near-infrared) induced imaging and regioselective cell killing. Chem Comm. 2010;46:6678-80.
17. Maiti KK, Lee WS, Takeuchi T, Watkins C, Fretz M, Kim D-C, et al. Guanidine-containing molecular transporters: sorbitol-based transporters show high intracellular selectivity toward mitochondria. Angew Chem Int Ed. 2007;46:5880-4. (Pubitemid 47236461)
18. Sibrian-Vazquez M, Nesterova IV, Jensen TJ, Vicente MGH. Mitochondria targeting by guanidine- and biguanidine-porphyrin photosensitizers. Bioconjugate Chem. 2008;19:705-13. (Pubitemid 351431403)
19. Fernández-Carneado J, Van Gool M, Martos V, Castel S, Prados P, de Mendoza J, et al. Highly efficient, nonpeptidic oligoguanidinium vectors that selectively internalize into mitochondria. J Am Chem Soc. 2005;127:869-74. (Pubitemid 40144285)
20. Biswas G, Jeon O-Y, Lee WS, Kim D-C, Kim K-T, Lee S, et al. Novel guanidine-containing molecular transporters based on lactose scaffolds: lipophilicity effect on the intracellular organellar selectivity. Chem Eur J. 2008;14:9161-8.
21. Zhao K, Zhao G-M, Wu D, Soong Y, Birk AV, Schiller PW, et al. Cell-permeable peptide antioxidants targeted to inner mitochondrial membrane inhibit mitochondrial swelling, oxidative cell death, and reperfusion injury. J Biol Chem. 2004;279:34682-90. (Pubitemid 39318098)
22. Szeto HH. Cell-permeable, mitochondrial-targeted, peptide antioxidants. AAPS J. 2006;8:E277-83.
23. Horton KL, Stewart KM, Fonseca SB, Guo Q, Kelley SO. Mitochondria- penetrating peptides. Chem Biol. 2008;15:375-82. (Pubitemid 351508434)
24. Yousif LF, Stewart KM, Horton KL, Kelley SO. Mitochondriapenetrating peptides: sequence effects and model cargo transport. ChemBioChem. 2009;10:2081-8.
25. Yousif LF, Stewart KM, Kelley SO. Targeting mitochondria with organelle-specific compounds: strategies and applications. Chem- BioChem. 2009;10:1939-50.
26. Horton KL, Kelley SO. Engineered apoptosis-inducing peptides with enhanced mitochondrial localization and potency. J Med Chem. 2009;52:3293-9.
27. MahonKP, Potocky TB, BlairD, RoyMD, StewartKM, Chiles TC, et al. Deconvolution of the cellular oxidative stress response with organelle-specific peptide conjugates. Chem Biol. 2007;14:923-30. (Pubitemid 47268781)
28. Pereira MP, Kelley SO. Maximizing the therapeutic window of an antimicrobial drug by impartig mitochondrial sequestration in human cells. J Am Chem Soc. 2011;133:3260-3.
29. Del Gaizo V, Payne RM. A novel TAT-mitochondrial signal sequence fusion protein is processed, stays in mitochondria, and crosses the placenta. Mol Ther. 2003;7:720-30. (Pubitemid 36790248)
30. Mukhopadhyay A, Ni L, Yang CS,Weiner H. Bacterial signal peptide recognizes HeLa cell mitochondrial import receptors and functions as a mitochondrial leader sequence. CMLS. 2005;62:1890-9. (Pubitemid 41188528)
31. Flierl A, Jackson C, Cottrell B, Murdock D, Seibel P, Wallace DC. Targeted delivery of DNA to the mitochondrial compartment via import sequence-conjugated peptide nucleic acid. Mol Ther. 2003;7:550-7. (Pubitemid 36553425)
32. Lamla M, Seliger H, Kaufmann D. Differences in uptake, localization, and processing of PNAs modified by COX VIII pre-sequence peptide and by triphenylphoshonium cation into mitochondria of tumor cells. Drug Deliv. 2010;17:263-71.
33. Fetisova EK, Avetisyan AV, Izyumov DS, Korotetskaya MV, Chernyak BV, Skulachev VP. Mitochondria-targeted antioxidant SkQR1 selectively protects MDR (Pgp 170)-negative cells against oxidative stress. FEBS Lett. 2010;584:562-6.
34. Brown SE, Ross MF, Sanjuan-Pla A, Manas A-RB, Smith RAJ, Murphy MP. Targeting lipoic acid to mitochondria: synthesis and characterization of a triphenylphosphonium-conjugated α-lipoyl derivative. Free Rad Biol Med. 2007;42:1766-80. (Pubitemid 46759581)
35. Mattarei A, Biasutto L, Marotta E, De MarchiU, Sassi N,Garbisa S, et al. A mitochondriotropic derivative of Quercetin: a strategy to increase the effectiveness of polyphenols. ChemBioChem. 2008;9:2633-42.
36. Asin-Cayuela J, Manas A-RB, James AM, Smith RAJ, Murphy MP. Fine-tuning the hydrophobicity of a mitochondria-targeted antioxidant. FEBS Lett. 2004;571:9-16. (Pubitemid 38992915)
37. Murphy MP, Smith RAJ. Targeting antioxidants to mitochondria by conjugation to lipophilic cations. Annu Rev Pharmacol Toxicol. 2007;47:629-56.
38. BiasuttoL,Mattarei A,MarottaE,BradaschiaA, SassiN,GarbisaS, et al. Development of mitochondria-targeted derivatives of resveratrol. Bioorg Med Chem Lett. 2008;18:5594-7.
39. Modica-Napolitano JS, Aprille JR. Delocalized lipophilic cations selectively target the mitochondria of carcinoma cells. Adv Drug Del Rev. 2001;49:63-70. (Pubitemid 32493800)
40. Fantin VR, Leder P. Mitochondriotoxic compounds for cancer therapy. Oncogene. 2006;25:4787-97. (Pubitemid 44187626)
41. Huang Z, Jiang J, Belikova N, Stoyanovsky D, Kagan V, Mintz A. Protection of normal brain cells from γ-irradiation-induced apoptosis by a mitochondria-targeted triphenyl-phosphonium-nitroxide: a possible utility in glioblastoma therapy. J Neurooncol. 2010;100:1-8.
42. Porteous CM, Logan A, Evans C, Ledgerwood EC, Menon DK, Aigbirhio F, et al. Rapid uptake of lipophilic triphenylphosphonium cations by mitochondria in vivo following intravenous injection: Implications for mitochondria-specific therapies and probes. Biochim Biophys Acta. 2010;1800:1009-17.
43. Prime TA, Blaikie FH, Evans C, Nadtochiy SM, James AM, Dahm CC, et al. A mitochondria-targeted S-nitrosothiol modulates respiration, nitrosates thiols, and protects against ischemiareperfusion injury. Proc Natl Acad Sci USA. 2009;106:10764-9.
44. Belikova NA, Jiang J, Stoyanovsky DA, Glumac A, Bayir H, Greenberger JS, et al. Mitochondria-targeted (2-hydroxyaminovinyl)- triphenyl-phosphonium releases NO and protects mouse embryonic cells against irradiation-induced apoptosis. FEBS Lett. 2009;583:1945-50.
45. Smith RAJ, Porteous CM, Gane AM, Murphy MP. Delivery of bioactive molecules to mitochondria in-vivo. Proc Natl Acad Sci USA. 2003;100:5407-12. (Pubitemid 36542718)
46. Ross MF, Filipovska A, Smith RAJ, Gait MJ, Murphy MP. Cellpenetrating peptides do not cross mitochondrial membranes even when conjugated to a lipophilic cation: evidence against direct passage through phospholipid bilayers. Biochem J. 2004;383:457-68. (Pubitemid 39546115)
47. Duca M, Dozza B, Lucarelli E, Santi S, Di Giorgio A, Barbarella G. Fluorescent labeling of human mesenchymal stem cells by thiophene fluorophores conjugated to a lipophilic carrier. Chem Comm. 2010;46:7948-50.
48. KooC-K, So LK-Y, Wong K-L,Ho Y-M, LamY-W, LamMHW, et al. A Triphenylphosphonium-functionalised cyclometalated platinum(II) complex as a nucleolus-specific two-photon molecular dye. Chem Eur J. 2010;16:3942-50.
49. Abu-Gosh SE, Kolvazon N, Tirosh B, Ringel I, Yavin E. Multiple Triphenylphosphonium cations shuttle a hydrophilic peptide into mitochondria. Mol Pharm. 2009;6:1138-44.
50. Javadpour MM, Juban MM, Lo W-CJ, Bishop SM, Alberty JB, Cowell SM, et al. novo antimicrobial peptides with low mammalian cell toxicity. J Med Chem. 1996;39:3107-13. (Pubitemid 26260315)
51. Ellerby HM, Arap W, Ellerby LM, Kain R, Andrusiak R, Rio GD, et al. Anti-cancer activity of targeted pro-apoptotic peptides. Nature Med. 1999;5:1032-8. (Pubitemid 29439574)
52. Fantin VR, Berardi MJ, Babbe H, Michelman MV, Manning CM, Leder P. A bifunctional targeted peptide that blocks HER-2 tyrosine kinase and disables mitochondrial function in HER-2- positive carcinoma cells. Cancer Res. 2005;65:6891-900. (Pubitemid 41060728)
53. Foillard S, Jin Z-h, Garanger E, Boturyn D, Favrot M-C, Coll JL, et al. Synthesis and biological characterisation of targeted proapoptotic peptide. ChemBioChem. 2008;9:2326-32.
54. Watkins CL, Brennan P, Fegan C, Takayama K, Nakase I, Futaki S, et al. Cellular uptake, distribution and cytotoxicity of the hydrophobic cell penetrating peptide sequence PFVYLI linked to the proapoptotic domain peptide PAD. J Controlled Rel. 2009;140:237-44.
55. Cai H, Yang H, Xiang B, Li S, Liu S, Wan L, et al. Selective apoptotic killing of solid and hematologic tumor cells by Bombesin-targeted delivery of mitochondria-disrupting peptides. Mol Pharm. 2010;7:586-96.
56. Lemeshko VV. Potential-dependent membrane permeabilization and mitochondrial aggregation caused by anticancer polyarginine- KLA peptides. Arch Biochem Biophys. 2010;493:213-20.
57. Angeles-Boza AM, Erazo-Oliveras A, Lee Y-J, Pellois J-P. Generation of endosomolytic reagents by branching of cell-penetrating peptides: tools for the delivery of bioactive compounds to live cells in cis or trans. Bioconjugate Chem. 2010;21:2164-7.
58. Khandazhinskaya AL, Kukhanova MK, Jasko MV. New nonnucleoside substrates for terminal deoxynucleotidyl transferase: synthesis and dependence of substrate properties on structure. Russian J Bioorg Chem. 2005;31:352-6. (Pubitemid 41204454)
59. Zhoua P, Dragulescu-Andrasia A, Bhattacharyab B, O'Keefeb H, Vattab P, Hyldig-Nielsenb JJ, et al. Synthesis of cellpermeable peptide nucleic acids and characterization of their hybridization and uptake properties. Bioorg Med Chem Lett. 2006;16:4931-5.
60. Jullian M, Hernandez A, Maurras A, Puget K, Amblard M, Martinez J, et al. N-terminus FITC labeling of peptides on solid support: the truth behind the spacer. Tetrahedron Lett. 2009;50:260-3.
61. Koning AJ, Lum PY, Williams JM, Wright R. DiOC6 staining reveals organelle structure and dynamics in living yeast cells. Cell Motil Cytoskeleton. 1993;25:111-28. (Pubitemid 23163165)