Enhancement of the uptake and cytotoxic activity of doxorubicin in cancer cells by novel cRGD-semipeptide-anchoring liposomes

Molecular Pharmaceutics

Volumn 11, Issue 7, 2014, Pages 2280-2293

  Battistini, Lucia ^a   Burreddu, Paola ^b   Sartori, Andrea ^a   Arosio, Daniela ^b   Manzoni, Leonardo ^b   Paduano, Luigi ^c,d   Derrico, Gerardino ^c,d   Sala, Roberto ^a   Reia, Laura ^a   Bonomini, Sabrina ^a   Rassu, Gloria ^b   Zanardi, Franca ^a  

^a UNIVERSITY OF PARMA   (Italy)

^b CNR   (Italy)

^c UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^d Dipartimento di Scienze Chimiche Università Degli Studi di Napoli Federico II ^*  (Italy)

Author keywords

drug delivery; integrin ligands; liposomes; nanoparticles; RGD semipeptides

Indexed keywords

ALKANE DERIVATIVE; DOXORUBICIN; DRUG CARRIER; LIPOSOME; NANOPARTICLE; PROLINE DERIVATIVE; VITRONECTIN RECEPTOR; ANTINEOPLASTIC AGENT; ARGINYL-GLYCYL-ASPARTIC ACID; OLIGOPEPTIDE;

ARTICLE; BREAST ADENOCARCINOMA; CELL DEATH; CELL POPULATION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOTOXICITY; DRUG DELIVERY SYSTEM; DRUG FORMULATION; DRUG POTENCY; DRUG UPTAKE; ELECTRON SPIN RESONANCE; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; IC 50; IN VITRO STUDY; LIGHT SCATTERING; MCF 7 CELL LINE; NANOENCAPSULATION; NEUTRON SCATTERING; PARTICLE SIZE; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; SYNTHESIS; BREAST NEOPLASMS; CELL NUCLEUS; CHEMISTRY; DRUG EFFECTS; FEMALE; METABOLISM; PROCEDURES; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CELL DEATH; CELL LINE, TUMOR; CELL NUCLEUS; DOXORUBICIN; DRUG DELIVERY SYSTEMS; FEMALE; HUMANS; LIPOSOMES; MCF-7 CELLS; NANOPARTICLES; OLIGOPEPTIDES; PARTICLE SIZE;

EID: 84903955086     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp400718j     Document Type: Article

References (54)

1. Kamaly, N.; Xiao, Z.; Valencia, P. M.; Radovic-Moreno, A. F.; Farokhzad, O. C. Targeted polymeric therapeutic nanoparticles: design, development and clinical translation Chem. Soc. Rev. 2012, 41, 2971-3010
2. Doane, T. L.; Burda, C. The unique role of nanoparticles in nanomedicine: imaging, drug delivery and therapy Chem. Soc. Rev. 2012, 41, 2885-2911
3. Cabral, O.; Nishiyama, N.; Kataoka, K. Supramolecular nanodevices: from design validation to theranostic nanomedicine Acc. Chem. Res. 2011, 44, 999-1008
4. Khemtong, C.; Kessinger, C. W.; Gao, J. Polymeric nanomedicine for cancer MR imaging and drug delivery Chem. Commun. 2009, 3497-3510
5. Richemann, K.; Schneider, S. W.; Luger, T. A.; Godin, B.; Ferrari, M.; Fuchs, H. Nanomedicine: challenge and perspectives Angew. Chem., Int. Ed. 2009, 48, 872-897
6. Ferrari, M. Cancer nanotechnology: opportunities and challenges Nat. Rev. Cancer 2005, 5, 161-171
7. Arosio, D.; Casagrande, C.; Manzoni, L. Integrin-mediated drug delivery in cancer and cardiovascular diseases with peptide-functionalized nanoparticles Curr. Med. Chem. 2012, 19, 3128-3151
8. Gunasekera, U. A.; Pankhurst, Q. A.; Douek, M. Imaging applications of nanotechnology in cancer Target Oncol. 2009, 4, 169-181
9. Zhao, P.; Astruc, D. Docetaxel nanotechnology in anticancer therapy ChemMedChem 2012, 7, 952-972
10. Paliwal, S. R.; Paliwal, R.; Agrawal, G. P.; Vyas, S. P. Liposomal nanomedicine for breast cancer therapy Nanomedicine 2011, 6, 1085-1100
11. Line, B. R.; Mitra, A.; Nan, A.; Ghandehari, H. Targeting tumor angiogenesis: comparison of peptides and polymer-peptide conjugates J. Nucl. Med. 2005, 46, 1552-1560
12. Iyer, A. K.; Khaled, G.; Fang, J.; Maeda, H. Exploiting the enhanced permeability and retention effect for tumor targeting Drug Discovery Today 2006, 11, 812-818
13. Elsabahy, M.; Wooley, K. L. Design of polymeric nanoparticles for biomedical delivery applications Chem. Soc. Rev. 2012, 41, 2545-2561
14. Allen, T. M.; Cullis, P. R. Liposomal drug delivery systems: from concepts to clinical applications Adv. Drug Delivery Rev. 2013, 65, 36-48
15. Desgrosselier, J. S.; Cheresh, D. A. Integrins in cancer: biological implications and therapeutic opportunities Nat. Rev. Cancer 2010, 10, 9-22
16. 3 integrin for a new cancer therapy Angew. Chem., Int. Ed. 1997, 36, 1374-1389
17. 3 integrin: design and applications of mono- and multifunctional RGD-based peptides and semipeptides Curr. Med. Chem. 2010, 17, 1255-1299
18. Manzoni, L.; Belvisi, L.; Arosio, D.; Civera, M.; Pilkington-Miksa, M.; Potenza, D.; Caprini, A.; Araldi, E. M. V.; Monferini, E.; Mancino, M.; Podestà, F.; Scolastico, C. Cyclic RGD-containing functionalized azabicycloalkane peptides as potent integrin antagonists for tumor targeting ChemMedChem 2009, 4, 615-632
19. Battistini, L.; Burreddu, P.; Carta, P.; Rassu, G.; Auzzas, L.; Curti, C.; Zanardi, F.; Manzoni, L.; Araldi, E. M. V.; Scolastico, C.; Casiraghi, G. 4-Aminoproline-based arginine-glycine-aspartate integrin binders with exposed ligation points: practical in-solution synthesis, conjugation and binding affinity evaluation Org. Biomol. Chem. 2009, 7, 4924-4935
20. Pilkington-Miksa, M.; Arosio, D.; Battistini, L.; Belvisi, L.; De Matteo, M.; Vasile, F.; Burreddu, P.; Carta, P.; Rassu, G.; Perego, P.; Carenini, N.; Zunino, F.; De Cesare, M.; Castiglioni, V.; Scanziani, E.; Scolastico, C.; Casiraghi, G.; Zanardi, F.; Manzoni, L. Design, synthesis and biological evaluation of novel cRGD-paclitaxel conjugates for integrin-assisted drug delivery Bioconjugate Chem. 2012, 23, 1610-1622
21. 3 integrin in glioblastoma xenografts Contrast Media Mol. Imaging 2011, 6, 449-458
22. Manzoni, L.; Belvisi, L.; Arosio, D.; Bartolomeo, M. P.; Bianchi, A.; Brioschi, C.; Buonsanti, F.; Cabella, C.; Casagrande, C.; Civera, M.; De Matteo, M.; Fugazza, L.; Lattuada, L.; Maisano, F.; Miragoli, L.; Neira, C.; Pilkington-Miksa, M.; Scolastico, C. Synthesis of Gd and (68)Ga complexes in conjugation with a conformationally optimized RGD sequence as potential MRI and PET tumor-imaging probes ChemMedChem 2012, 7, 1084-1093
23. Drago, C.; Arosio, D.; Casagrande, C.; Manzoni, L. Bisphosphonate- functionalized cyclic Arg-Gly-Asp peptidomimetics Arkivoc 2013, 12, 185-200
24. 68Ga-NOTA-RGD peptidomimetic conjugate in rat myocardial infarction Eur. J. Nucl. Med. Mol. Imaging 2013, 40, 1265-1274
25. Accardo, A.; Tesauro, D.; Roscigno, P.; Gianolio, E.; Paduano, L.; DErrico, G.; Pedone, C.; Morelli, G. Physicochemical properties of mixed micellar aggregates containing CCK peptides and Gd complexes designed as tumor specific contrast agents in MRI J. Am. Chem. Soc. 2004, 26, 3097-3107
26. Vaccaro, M.; Accardo, A.; Tesauro, D.; Mangiapia, G.; Löf, D.; Schillén, K.; Söderman, O.; Morelli, G.; Paduano, L. Supramolecular aggregates of amphiphilic gadolinium complexes as blood pool MRI/MRA contrast agents: physicochemical characterization Langmuir 2006, 22, 6635-6643
27. Niu, G.; Cogburn, B.; Hughes, J. Preparation and Characterization of Doxorubicin Liposomes. In Cancer Nanotechnology (Methods in Molecular Biology); Grobmyer, S. R.; Moudgil, B. M., Eds.; Springer: New York, 2010; Vol. 624, pp 211-219.
28. Heenan, R. K.; Penfold, J.; King, S. M. SANS at pulsed neutron sources: present and future prospects J. Appl. Crystallogr. 1997, 30, 1140-1147
29. Wignall, G. D.; Bates, F. S. Absolute calibration of small-angle neutron scattering data J. Appl. Crystallogr. 1987, 20, 28-40
30. Narita, T.; Kimura, N.; Sato, M.; Matsuura, N.; Kannagi, R. Altered expression of integrins in adriamycin-resistant human breast cancer cells Anticancer Res. 1998, 18, 257-262
31. Nejjari, M.; Hafdi, Z.; Gouysse, G.; Fiorentino, M.; Béatrix, O.; Dumortier, J.; Pourreyron, C.; Barozzi, C.; DErrico, A.; Grigioni, W. F.; Scoazec, J. Y. Expression, regulation, and function of alpha V integrins in hepatocellular carcinoma: an in vivo and in vitro study Hepatology 2002, 36, 418-426
32. DErrico, 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
33. Arzillo, M.; Mangiapia, G.; Pezzella, A.; Heenan, R. K.; Radulescu, A.; Paduano, L.; DIschia, M. Eumelanin buildup on the nanoscale: aggregate growth/assembly and visible absorption development in biomimetic 5,6-dihydroxyindole polymerization Biomacromolecules 2012, 13, 2379-2390
34. Vergara, A.; Paduano, L.; Vitagliano, V.; Sartorio, R. Mutual diffusion in aqueous solution of poly(ethyleneglycol) samples. Some comments on the effect of chain length and polydispersity Phys. Chem. Chem. Phys. 1999, 1, 5377-5383
35. Mangiapia, G.; Vaccaro, M.; DErrico, 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
36. Busi, E.; Vitiello, G.; Niccoli, M.; Basosi, R.; Montesarchio, D.; DErrico, G. On the mechanism of ion transport through lipid membranes mediated by PEGylated cyclic oligosaccharides (CyPLOS): an ESR study Biochim. Biophys. Acta, Biomembr. 2013, 1828, 2074-2082
37. Vitiello, G.; Falanga, A.; Galdiero, M.; Marsh, D.; Galdiero, S.; DErrico, G. Lipid composition modulates the interaction of peptides deriving from herpes simplex virus type I glycoproteins B and H with biomembranes Biochim. Biophys. Acta, Biomembr. 2011, 1808, 2517-2526
38. Galdiero, S.; Falanga, A.; Vitiello, G.; Vitiello, M.; Pedone, C.; DErrico, 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
39. Zhao, H.; Wang, J. C.; Sun, Q. S.; Luo, C. L.; Zhang, Q. RGD-based strategies for improving antitumor activity of paclitaxel-loaded liposomes in nude mice xenografted with human ovarian cancer J. Drug Targeting 2009, 17, 10-18
40. Dubey, P. K.; Mishra, V.; Jain, S.; Mahor, S.; Vyas, S. P. Liposomes modified with cyclic RGD peptide for tumor targeting J. Drug Targeting 2004, 12, 257-264
41. Hölig, P.; Bach, M.; Völkel, T.; Nahde, T.; Hoffmann, S.; Müller, R.; Kontermann, R. E. Novel RGD lipopeptides for the targeting of liposomes to integrin-expressing endothelial and melanoma cells Protein Eng., Des. Sel. 2004, 17, 433-441
42. Xiong, X.-B.; Huang, Y.; Lu, W.-L.; Zhang, X.; Zhang, H.; Nagai, T.; Zhang, Q. Enhanced intracellular delivery and improved antitumor efficacy of doxorubicin by sterically stabilized liposomes modified with a synthetic RGD mimetic J. Controlled Release 2005, 107, 262-275
43. Xiong, X.-B.; Huang, Y.; Lu, W.-L.; Zhang, X.; Zhang, H.; Nagai, T.; Zhang, Q. Intracellular delivery of doxorubicin with RGD-modified sterically stabilized liposomes for an improved antitumor efficacy: in vitro and in vivo J. Pharm. Sci. 2005, 94, 1782-1793
44. Fens, M. H. A. M.; Hill, K. J.; Ashton, S. E.; Westwood, F. R.; Blakey, D. C.; Storm, G.; Ryan, A. J.; Schiffelers, R. M. Liposomal encapsulation enhances the antitumor efficacy of the vascular disrupting ZD6126 in murine B16.F10 melanoma Br. J. Cancer 2008, 99, 1256-1264
45. Murphy, E. A.; Majeti, B. K.; Barnes, L. A.; Makale, M.; Weis, S. M.; Lutu-Fuga, K.; Wrasidlo, W.; Cheresh, D. A. Nanoparticle-mediated drug delivery to tumor vasculature suppresses metastasis Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 9343-9348
46. Cressman, S.; Dobson, I.; Lee, J. B.; Tam, Y. Y. C.; Cullis, P. R. Synthesis of a labeled RGD-lipid. Its incorporation into liposomal nanoparticles, and their trafficking in cultured endothelial cells Bioconjugate Chem. 2009, 20, 1404-1411
47. Meng, S.; Su, B.; Ding, Y.; Tang, L.; Zhou, W.; Song, Y.; Li, H.; Zhou, C. Enhanced antitumor effect of novel dual-targeted paclitaxel liposomes Nanotechnology 2010, 21, 415103
48. Düzgünes, N.; Nir, S. Mechanisms and kinetics of liposome-cell interactions Adv. Drug Delivery Rev. 1999, 40, 3-18
49. Bareford, L. M.; Swaan, P. W. Endocytic mechanisms for targeted drug delivery Adv. Drug Delivery Rev. 2007, 59, 748-758
50. Breunig, M.; Bauer, A.; Goepferich, A. Polymers and nanoparticles: intelligent tools for intracellular targeting? Eur. J. Pharm. Biopharm. 2008, 68, 112-128
51. des Rieux, A.; Fievez, V.; Garinot, M.; Schenider, Y. J.; Préat, V. Nanoparticles as potential oral delivery systems of proteins and vaccines: a mechanistic approach J. Controlled Release 2006, 116, 1-27
52. Masunaga, S.; Ono, K. Significance of the response of quiescent cell population within solid tumors in cancer therapy J. Radiat. Res. 2002, 43, 11-25
53. Lou, P.-J.; Lai, P.-S.; Shieh, M.-J. A.; MacRobert, J.; Berg, K.; Bown, S. G. Reversal of doxorubicin resistance in breast cancer cells by photochemical internalization Int. J. Cancer 2006, 119, 2692-2698
54. Masunaga, S.-I.; Kono, K.; Nakamura, J.; Tano, K.; Yoshida, H.; Watanabe, M.; Kashino, G.; Suzuki, M.; Kinashi, Y.; Liu, Y.; Ono, K. Usefulness of hexamethylenetetramine in combination with chemotherapy using free and pegylated liposomal doxorubicin in vivo, referring to the effect on quiescent cells Oncol. Rep. 2009, 21, 1307-1312