Anticancer cationic ruthenium nanovectors: From rational molecular design to cellular uptake and bioactivity

Biomacromolecules

Volumn 14, Issue 8, 2013, Pages 2549-2560

  Mangiapia, Gaetano ^a,b   Vitiello, Giuseppe ^a,b   Irace, Carlo ^a   Santamaria, Rita ^a   Colonna, Alfredo ^a   Angelico, Ruggero ^b,c   Radulescu, Aurel ^d   D'Errico, Gerardino ^a,b   Montesarchio, Daniela ^a   Paduano, Luigi ^a,b  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b UNIVERSITY OF FLORENCE   (Italy)

^c DISTAAM   (Italy)

^d Forschungszentrum   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOCARCINOMA CELLS; EFFICIENT DRUG DELIVERY; ELECTRON PARAMAGNETIC RESONANCES (EPR); IN-VITRO BIOACTIVITY; MICRO-STRUCTURAL CHARACTERIZATION; NEUTRON REFLECTIVITY; SMALL-ANGLE NEUTRON SCATTERING; ZETA POTENTIAL MEASUREMENTS;

CELL CULTURE; CHLORINE COMPOUNDS; DRUG DELIVERY; DYNAMIC LIGHT SCATTERING; FLUORESCENCE MICROSCOPY; HYDROGELS; MAGNETIC RESONANCE; NANOPARTICLES; PARAMAGNETISM; PHOSPHOLIPIDS; RUTHENIUM; SYNTHESIS (CHEMICAL);

RUTHENIUM COMPOUNDS;

1,2 DIOLEOYL 3 TRIMETHYLAMMONIOPROPANE; 1,2 DIOLEOYL 3 TRIMETHYLAMMONIOPROPANE RUTHENIUM COMPLEX; ANTINEOPLASTIC AGENT; DRUG CARRIER; NANOPARTICLE; RHODAMINE B; RUTHENIUM; RUTHENIUM COMPLEX; UNCLASSIFIED DRUG; ALLYL COMPOUND; COLLOID; COORDINATION COMPOUND; LIPID; LIPOSOME; SURFACTANT;

ANIMAL CELL; ARTICLE; BIOLOGICAL ACTIVITY; CANCER CELL CULTURE; CELL STRAIN MCF 7; CELL TRANSPORT; CONTROLLED STUDY; CYTOTOXICITY; DRUG DELIVERY SYSTEM; DRUG DESIGN; DRUG FORMULATION; DRUG STABILITY; DRUG UPTAKE; ELECTRON SPIN RESONANCE; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; IC 50; IN VITRO STUDY; LIGHT SCATTERING; NEUTRON REFLECTIVITY; NEUTRON SCATTERING; NONHUMAN; PRIORITY JOURNAL; PROCEDURES; RAT; ANIMAL; CELL SURVIVAL; CHEMISTRY; COLLOID; DRUG EFFECTS; DRUG SCREENING; HALF LIFE TIME; IC50; MCF 7 CELL LINE; METABOLISM; NEUTRON DIFFRACTION; PARTICLE SIZE; SMALL ANGLE SCATTERING;

ALLYL COMPOUNDS; ANIMALS; ANTINEOPLASTIC AGENTS; CELL SURVIVAL; COLLOIDS; COORDINATION COMPLEXES; DRUG SCREENING ASSAYS, ANTITUMOR; DRUG STABILITY; ELECTRON SPIN RESONANCE SPECTROSCOPY; HALF-LIFE; HUMANS; INHIBITORY CONCENTRATION 50; LIPIDS; LIPOSOMES; MCF-7 CELLS; NANOPARTICLES; NEUTRON DIFFRACTION; PARTICLE SIZE; RUTHENIUM; SCATTERING, SMALL ANGLE; SURFACE-ACTIVE AGENTS;

EID: 84881575120     PISSN: 15257797     EISSN: 15264602     Source Type: Journal    
DOI: 10.1021/bm400104b     Document Type: Article

References (51)

1. Rosenberg, B.; Van Camp, L.; Krigas, T. Inhibition of cell division in Escherichia coli by electrolysis products from a platinum electrode Nature (London, U. K.) 1965, 205, 698-9
2. Kelland, L. The resurgence of platinum-based cancer chemotherapy Nat. Rev. Cancer 2007, 7, 573-584
3. Drayton, R. M.; Catto, J. W. F. Molecular mechanisms of cisplatin resistance in bladder cancer Expert Rev. Anticancer 2012, 12, 271-281
4. Yao, X.; Panichpisal, K.; Kurtzman, N.; Nugent, K. Cisplatin nephrotoxicity: A review Am. J. Med. Sci. 2007, 334, 115-124
5. Levina, A.; Mitra, A.; Lay, P. A. Recent developments in ruthenium anticancer drugs Metallomics 2009, 1, 458-470
6. Bergamo, A.; Gaiddon, C.; Schellens, J. H. M.; Beijnen, J. H.; Sava, G. Approaching tumour therapy beyond platinum drugs Status of the art and perspectives of ruthenium drug candidates J. Inorg. Biochem. 2012, 106, 90-99
7. Alessio, E.; Mestroni, G.; Bergamo, A.; Sava, G. Ruthenium antimetastatic agents Curr. Top. Med. Chem. 2004, 4, 1525-1535
8. Lentz, F.; Drescher, A.; Lindauer, A.; Henke, M.; Hilger, R. A.; Hartinger, C. G.; Scheulen, M. E.; Dittrich, C.; Keppler, B. K.; Jaehde, U. Pharmacokinetics of a novel anticancer ruthenium complex (KP1019, FFC14A) in a phase I dose-escalation study Anti-Cancer Drug 2009, 20, 97-103
9. Bouma, M.; Nuijen, B.; Jansen, M. T.; Sava, G.; Flaibani, A.; Bult, A.; Beijnen, J. H. A kinetic study of the chemical stability of the antimetastatic ruthenium complex NAMI-A Int. J. Pharm. 2002, 248, 239-246
10. Mangiapia, G.; D'Errico, G.; Simeone, L.; Irace, C.; Radulescu, A.; Di Pascale, A.; Colonna, A.; Montesarchio, D.; Paduano, L. Ruthenium-based complex nanocarriers for cancer therapy Biomaterials 2012, 33, 3770-3782
11. Lasic, D. D.; Woodle, M. C.; Martin, F. J.; Valentincic, T. Phase-behavior of stealth-lipid-lecithin mixtures Period. Biol. 1991, 93, 287-290
12. Vaccaro, M.; Del Litto, R.; Mangiapia, G.; Carnerup, A. M.; D'Errico, G.; Ruffo, F.; Paduano, L. Lipid based nanovectors containing ruthenium complexes: a potential route in cancer therapy Chem. Commun. 2009, 1404-1406
13. Mangiapia, G.; Vaccaro, M.; D'Errico, G.; Frielinghaus, H.; Radulescu, A.; Pipich, V.; Carnerup, A. M.; Paduano, L. Cubosomes for ruthenium complex delivery: formulation and characterization Soft Matter 2011, 7, 10577-10580
14. D'Errico, G.; Silipo, A.; Mangiapia, G.; Vitiello, G.; Radulescu, A.; Molinaro, A.; Lanzetta, R.; Paduano, L. Characterization of liposomes formed by lipopolysaccharides from Burkholderia cenocepacia, Burkholderia multivorans, and Agrobacterium tumefaciens: from the molecular structure to the aggregate architecture Phys. Chem. Chem. Phys. 2010, 12, 13574-13585
15. Simeone, L.; Mangiapia, G.; Irace, C.; Di Pascale, A.; Colonna, A.; Ortona, O.; De Napoli, L.; Montesarchio, D.; Paduano, L. Nucleolipid nanovectors as molecular carriers for potential applications in drug delivery Mol. Biosyst. 2011, 7, 3075-3086
16. Coppola, C.; Paciello, A.; Mangiapia, G.; Licen, S.; Boccalon, M.; De Napoli, L.; Paduano, L.; Tecilla, P.; Montesarchio, D. Design, synthesis and characterisation of a fluorescently labelled CyPLOS ionophore Chem.-Eur. J. 2010, 16, 13757-13772
17. Branchi, B.; Ceroni, P.; Balzani, V.; Bergamini, G.; Klarner, F. G.; Vogtle, F. Adducts between dansylated poly(propylene amine) dendrimers and anthracene clips mediated by Zn-II Ions: highly efficient photoinduced energy transfer Chem.-Eur. J. 2009, 15, 7876-7882
18. Montalti, M.; Prodi, L.; Zaccheroni, N.; Battistini, G.; Marcuz, S.; Mancin, F.; Rampazzo, E.; Tonellato, U. Size effect on the fluorescence properties of dansyl-doped silica nanoparticles Langmuir 2006, 22, 5877-5881
19. Pagliari, S.; Corradini, R.; Galaverna, G.; Sforza, S.; Dossena, A.; Montalti, M.; Prodi, L.; Zaccheroni, N.; Marchelli, R. Enantioselective fluorescence sensing of amino acids by modified cyclodextrins: Role of the cavity and sensing mechanism Chem.-Eur. J. 2004, 10, 2749-2758
20. Ueno, A.; Ikeda, A.; Ikeda, H.; Ikeda, T.; Toda, F. Fluorescent cyclodextrins responsive to molecules and metal ions. Fluorescence properties and inclusion phenomena of N-α-dansyl- l -lysine-β-cyclodextrin and monensin-incorporated N-α-dansyl- l -lysine-β-cyclodextrin J. Org. Chem. 1999, 64, 382-387
21. Simeone, L.; Irace, C.; Di Pascale, A.; Ciccarelli, D.; D'Errico, G.; Montesarchio, D. Synthesis, self-aggregation and bioactivity properties of a cationic aminoacyl surfactant, based on a new class of highly functionalized nucleolipids Eur. J. Med. Chem. 2012, 57, 429-440
22. Simeone, L.; Mangiapia, G.; Vitiello, G.; Irace, C.; Colonna, A.; Ortona, O.; Montesarchio, D.; Paduano, L. Cholesterol-based nucleolipid-ruthenium complex stabilized by lipid aggregates for antineoplastic therapy Bioconjugate Chem. 2012, 23, 758-770
23. Chasin, M.; Langer, R., Eds. Drugs and the Pharmaceutical Sciences, Vol. 45: Biodegradable Polymers as Drug Delivery Systems; CRC Press: New York, 1990; p 347.
24. Evans, D. F.; Wennerström, H. The Colloidal Domain: Where Physics, Chemistry, Biology, and Technology Meet. Wiley-VCH: New York, 1999; p 632.
25. Vaccaro, M.; Accardo, A.; Tesauro, D.; Mangiapia, G.; Lof, D.; Schillen, K.; Soderman, O.; Morelli, G.; Paduano, L. Supramolecular aggregates of amphiphilic gadolinium complexes as blood pool MRI/MRA contrast agents: physicochemical characterization Langmuir 2006, 22, 6635-43
26. Ma, G.; Barlow, D. J.; Lawrence, M. J.; Heenan, R. K.; Timmins, P. Small-angle neutron-scattering studies of nonionic surfactant vesicles J. Phys. Chem. B 2000, 104, 9081-9085
27. Pencer, J.; Krueger, S.; Adams, C. P.; Katsaras, J. Method of separated form factors for polydisperse vesicles J. Appl. Crystallogr. 2006, 39, 293-303
28. Kiselev, M. A.; Zemlyanaya, E. V.; Aswal, V. K.; Neubert, R. H. H. What can we learn about the lipid vesicle structure from the small-angle neutron scattering experiment? Eur. Biophys. J. 2006, 35, 477-493
29. Kotlarchyk, M.; Chen, S. H. Analysis of small angle neutron scattering spectra from polydisperse interacting colloids J. Chem. Phys. 1983, 79, 2461-9
30. Bartlett, P.; Ottewill, R. H.; Neutron-Scattering, A. Study of the structure of a bimodal colloidal crystal J. Chem. Phys. 1992, 96, 3306-3318
31. Vergara, A.; Paduano, L.; Sartorio, R. Multicomponent diffusion in systems containing molecules of different size. 4. Mutual diffusion in the ternary system tetra(ethylene glycol)-di(ethylene glycol)-water J. Phys. Chem. B 2001, 105, 328-334
32. Mangiapia, G.; Coppola, C.; Vitiello, G.; D'Errico, G.; De Napoli, L.; Radulescu, A.; Montesarchio, D.; Paduano, L. Nanostructuring of CyPLOS (cyclic phosphate-linked oligosaccharides), novel saccharide-based synthetic ion transporters J. Colloid Interface Sci. 2011, 354, 718-724
33. D'Errico, G.; Paduano, L.; Khan, A. Temperature and concentration effects on supramolecular aggregation and phase behavior for poly(propylene oxide)- b -poly(ethylene oxide)- b -poly(propylene oxide) copolymers of different composition in aqueous mixtures, 1 J. Colloid Interface Sci. 2004, 279, 379-390
34. D'Errico, G.; Paduano, L.; Ortona, O.; Mangiapia, G.; Coppola, L.; Lo Celso, F. Temperature and concentration effects on supramolecular aggregation and phase behavior for poly(propylene oxide)- b -poly(ethylene oxide)- b -poly(propylene oxide) copolymers of different concentration in aqueous mixtures, 2 J. Colloid Interface Sci. 2011, 359, 179-188
35. Hunter, R. J., Ed. Colloid Science: Zeta Potential in Colloid Science: Principles and Applications; Academic Press: New York, 1981; p 386.
36. Angelico, R.; Ambrosone, L.; Ceglie, A.; Losito, I.; De Zio, G.; Palmisano, F. Complementary amphiphilic ribonucleotides confined into nanostructured environments Phys. Chem. Chem. Phys. 2010, 12, 7977-7987
37. Kang, K.-H.; Kim, H.-U.; Lim, K.-H. Phase behavior and spontaneous vesicle formation in aqueous solutions of anionic ammonium dodecyl sulfate and cationic octadecyl trimethyl ammonium chloride surfactants Bull. Korean Chem. Soc. 2007, 28, 667-674
38. D'Errico, G.; D'Ursi, A. M.; Marsh, D. Interaction of a peptide derived from glycoprotein gp36 of feline immunodeficiency virus and its lipoylated analogue with phospholipid membranes Biochemistry 2008, 47, 5317-5327
39. D'Errico, G.; Vitiello, G.; Ortona, O.; Tedeschi, A.; Ramunno, A.; D'Ursi, A. M. Interaction between Alzheimer's A β(25-35) peptide and phospholipid bilayers: The role of cholesterol Biochim. Biophys. Acta, Biomembr. 2008, 1778, 2710-2716
40. Falanga, A.; Tarallo, R.; Vitiello, G.; Vitiello, M.; Perillo, E.; Cantisani, M.; D'Errico, G.; Galdiero, M.; Galdiero, S., Biophysical characterization and membrane interaction of the two fusion loops of glycoprotein B from herpes simplex type I virus. Plos One 2012, 7.
41. Spadaccini, R.; D'Errico, G.; D'Alessio, V.; Notomista, E.; Bianchi, A.; Merola, M.; Picone, D. Structural characterization of the transmembrane proximal region of the hepatitis C virus E1 glycoprotein Biochim. Biophys. Acta, Biomembr. 2010, 1798, 344-353
42. Galdiero, S.; Falanga, A.; Vitiello, G.; Vitiello, M.; Pedone, C.; D'Errico, G.; Galdiero, M. Role of membranotropic sequences from herpes simplex virus type I glycoproteins B and H in the fusion process Biochim. Biophys. Acta, Biomembr. 2010, 1798, 579-591
43. Tan, C. P.; Wu, S. H.; Lai, S. S.; Wang, M. X.; Chen, Y.; Zhou, L. J.; Zhu, Y. P.; Lian, W.; Peng, W. L.; Ji, L. N.; Xu, A. L. Synthesis, structures, cellular uptake and apoptosis-inducing properties of highly cytotoxic ruthenium-Norharman complexes Dalton Trans. 2011, 40, 8611-8621
44. Bailey, A. L.; Cullis, P. R. Membrane fusion with cationic liposomes: Effects of target membrane lipid composition Biochemistry 1997, 36, 1628-1634
45. Zabner, J.; Fasbender, A. J.; Moninger, T.; Poellinger, K. A.; Welsh, M. J. Cellular and molecular barriers to gene-transfer by a cationic lipid J. Biol. Chem. 1995, 270, 18997-19007
46. Grobben, B.; De Deyn, P. P.; Slegers, H. Rat C6 glioma as experimental model system for the study of glioblastoma growth and invasion Cell Tissue Res. 2002, 310, 257-270
47. Vergara, A.; D'Errico, G.; Montesarchio, D.; Mangiapia, G.; Paduano, L.; Merlino, A. Interaction of anticancer ruthenium compounds with proteins: high-resolution X-ray structures and raman microscopy studies of the adduct between hen egg white lysozyme and AziRu Inorg. Chem. 2013, 52, 4157-4159
48. Sava, G.; Bergamo, A.; Zorzet, S.; Gava, B.; Casarsa, C.; Cocchietto, M.; Furlani, A.; Scarcia, V.; Serli, B.; Iengo, E.; Alessio, E.; Mestroni, G. Influence of chemical stability on the activity of the antimetastasis ruthenium compound NAMI-A Eur. J. Cancer 2002, 38, 427-435
49. Galanski, M.; Keppler, B. K. Searching for the magic bullet: anticancer platinum drugs which can be accumulated or activated in the tumor tissue Anti-Cancer Agents Med. Chem. 2007, 7, 55-73
50. Tanford, C. Micelle Shape Size 1972, 76, 3020-3024
51. Mangiapia, G.; Accardo, A.; Lo Celso, F.; Tesauro, D.; Morelli, G.; Radulescu, A.; Paduano, L. Mixed micelles composed of peptides and gadolinium complexes as tumor-specific contrast agents in MRI: A SANS study J. Phys. Chem. B 2004, 108, 17611-17617