Improved anti-tumoral therapeutic efficacy of 4-hydroxynonenal incorporated in novel lipid nanocapsules in 2D and 3D models

Journal of Biomedical Nanotechnology

Volumn 11, Issue 12, 2015, Pages 2169-2185

  Pizzimenti, Stefania ^a   Daga, Martina ^a   Ciamporcero, Eric ^a   Toaldo, Cristina ^a   Pettazzoni, Piergiorgio ^a,d   Osella Abate, Simona ^b   Novelli, Mauro ^b   Minelli, Rosalba ^a   Bisazza, Agnese ^a   Gamba, Paola ^a   Testa, Gabriella ^a   Ullio, Chiara ^a   Ferruti, Paolo ^c   Ranucci, Elisabetta ^c   Bernengo, Maria Grazia ^b   Ferretti, Carlo ^a   Dianzani, Chiara ^a   Biasi, Fiorella ^a   Barrera, Giuseppina ^a   Cavalli, Roberta ^a  

^a UNIVERSITY OF TURIN   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

^d UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

4 hydroxynonenal; Human melanoma model; Lipid nanocapsules; Lipid peroxidation; Prolonged release; Tumour cell lines

Indexed keywords

CELL CULTURE; CELLS; CONTROLLED DRUG DELIVERY; DERMATOLOGY; LIPIDS; NANOCAPSULES; ONCOLOGY; OXIDATION; TARGETED DRUG DELIVERY; TUMORS;

4-HYDROXY-NONENAL; LIPID NANOCAPSULES; LIPID PEROXIDATION; PROLONGED RELEASE; TUMOUR CELLS;

THREE DIMENSIONAL COMPUTER GRAPHICS;

4 HYDROXYNONENAL; LIPID NANOCAPSULE; LIPOSOME; MEDIUM CHAIN TRIACYLGLYCEROL; NANOCARRIER; UNCLASSIFIED DRUG; 4-ACRYLOYLMORPHOLINE; 4-HYDROXY-2-NONENAL; ACRYLAMIDE DERIVATIVE; ALDEHYDE; CYCLODEXTRIN; DRUG CARRIER; LIPID; MORPHOLINE DERIVATIVE; NANOCAPSULE;

A375 CELL LINE; ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; CRITICAL MICELLE CONCENTRATION; CUTANEOUS MELANOMA; CYTOTOXICITY; DRUG EFFICACY; DRUG RELEASE; DRUG SAFETY; DRUG STABILITY; FLUORESCENCE; HL 60 CELL LINE; HT 29 CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; INTERNALIZATION; LIPID PEROXIDATION; LIPOPHILICITY; LIPOSOMAL DELIVERY; MALE; NANOFABRICATION; NANOPHARMACEUTICS; PROSTATE CANCER CELL LINE; SURFACE CHARGE; SURFACE TENSION; TOPICAL TREATMENT; U937 CELL LINE; UMBILICAL VEIN ENDOTHELIAL CELL; CHEMISTRY; DRUG EFFECTS; MELANOMA; PATHOLOGY; TRANSPORT AT THE CELLULAR LEVEL; TUMOR CELL LINE;

ACRYLAMIDES; ALDEHYDES; BIOLOGICAL TRANSPORT; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL PROLIFERATION; CYCLODEXTRINS; DRUG CARRIERS; DRUG STABILITY; HUMANS; LIPIDS; MELANOMA; MORPHOLINES; NANOCAPSULES;

EID: 84953344638     PISSN: 15507033     EISSN: 15507041     Source Type: Journal    
DOI: 10.1166/jbn.2015.2131     Document Type: Article

References (57)

1. G. Poli, R. J. Schaur, W. G. Siems, and G. Leonarduzzi, 4-hydroxynonenal: A membrane lipid oxidation product of medicinal interest. Med. Res. Rev. 28, 569 (2008).
2. G. Barrera, Oxidative stress and lipid peroxidation products in cancer progression and therapy. ISRN Oncol. 137289 (2012).
3. K. Uchida, 4-Hydroxy-2-nonenal: A product and mediator of oxidative stress. Prog. Lipid. Res. 42, 318 (2003).
4. G. Barrera, S. Pizzimenti, and M. U. Dianzani, Lipid peroxidation: Control of cell proliferation, cell differentiation and cell death. Mol. Aspects Med. 29, 1 (2008).
5. H. Esterbauer, R. J. Schaur, and H. Zollner, Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic. Biol. Med. 11, 81 (1991).
6. H. J. Forman, J. M. Fukuto, T. Miller, H. Zhang, A. Rinna, and S. Levy, The chemistry of cell signaling by reactive oxygen and nitrogen species and 4-hydroxynonenal. Arch. Biochem. Biophys. 477, 183 (2008).
7. V. P. Torchilin, Multifunctional nanocarriers. Adv. Drug. Deliv. Rev. 58, 1532 (2006).
8. I. Brigger, C. Dubernet, and P. Couvreur, Nanoparticles in cancer therapy and diagnosis. Adv. Drug Deliv. Rev. 54, 631 (2002).
9. Z. G. Chen, Small-molecule delivery by nanoparticles for anticancer therapy. Trends Mol. Med. 16, 594 (2010).
10. B. Mishra, B. B. Patel, and S. Tiwari, Colloidal nanocarriers: A review on formulation technology, types and applications toward targeted drug delivery. Nanomedicine 6, 9 (2009).
11. P. Couvreur, Nanoparticles in drug delivery: Past, present and future. Adv. Drug. Deliv. Rev. 65, 21 (2013).
12. R. Minelli, S. Occhipinti, C. L. Gigliotti, G. Barrera, P. Gasco, L. Conti, A. Chiocchetti, G. P. Zara, R. Fantozzi, M. Giovarelli, U. Dianzani, and C. Dianzani, Cholesteryl butyrate solid lipid nanoparticles inhibit the proliferation of cancer cells in vitro and in vivo models. Br. J. Pharmacol. 170, 233 (2013).
13. N. G. Eskandar, S. Simovic, and C. A. Prestidge, Chemical stability and phase distribution of all-trans-retinol in nanoparticle-coated emulsions. Int. J. Pharm. 376, 186 (2009).
14. N. Zhang, J. Li, W. Jiang, C. Ren, J. Xin, and K. Li, Effective protection and controlled release of insulin by cationic betacyclodextrin polymers from alginate/chitosan nanoparticles. Int. J. Pharm. 393, 212 (2010).
15. S. Swaminathan, L. Pastero, L. Serpe, F. Trotta, P. Vavia, D. Aquilano, M. Trotta, G. Zara, and R. Cavalli, Cyclodextrinbased nanosponges encapsulating camptothecin: Physicochemical characterization, stability and cytotoxicity. Eur. J. Pharm. Biopharm. 74, 193 (2010).
16. D. Hoarau, P. Delmas, S. David, E. Roux, and J. C. Leroux, Novel long-circulating lipid nanocapsules. Pharm. Res. 21, 1783 (2004).
17. N. T. Huynh, C. Passirani, P. Saulnier, and J. P. Benoit, Lipid nanocapsules: A new platform for nanomedicine. Int. J. Pharm. 379, 201 (2009).
18. C. G. Venturini, E. Jager, C. P. Oliveira, A. Bernardi, A. M. O. Battastini, S. S. Guterres, and A. R. Pohlmann, Formulation of lipid core nanocapsules. Colloids and Surfaces a-Physicochemical and Engineering Aspects 375, 200 (2011).
19. E. Roger, F. Lagarce, and J. P. Benoit, The gastrointestinal stability of lipid nanocapsules. Int. J. Pharm. 379, 260 (2009).
20. M. M. Abdel-Mottaleb, D. Neumann, and A. Lamprecht, Lipid nanocapsules for dermal application: A comparative study of lipidbased versus polymer-based nanocarriers. Eur. J. Pharm. Biopharm. 79, 36 (2011).
21. S. Hirsjarvi, S. Dufort, J. Gravier, I. Texier, Q. Yan, J. Bibette, L. Sancey, V. Josserand, C. Passirani, J. P. Benoit, and J. L. Coll, Influence of size, surface coating and fine chemical composition on the in vitro reactivity and in vivo biodistribution of lipid nanocapsules versus lipid nanoemulsions in cancer models. Nanomedicine 9, 375 (2012).
22. M. Bencini, E. Ranucci, P. Ferruti, F. Trotta, M. Donalisio, M. Cornaglia, D. Lembo, and R. Cavalli, Preparation and in vitro evaluation of the antiviral activity of the Acyclovir complex of a beta-cyclodextrin/poly(amidoamine) copolymer. J. Control. Release 126, 17 (2008).
23. R. Cavalli, M. Donalisio, A. Civra, P. Ferruti, E. Ranucci, F. Trotta, and D. Lembo, Enhanced antiviral activity of Acyclovir loaded into beta-cyclodextrin-poly(4-acryloylmorpholine) conjugate nanoparticles. J. Control. Release 137, 116 (2009).
24. R. J. Hunter and R. H. Ottewill, Zeta Potential in Colloid Science: Principles and Applications, Academic Press, London (1981).
25. M. D. Basson, G. A. Turowski, Z. Rashid, F. Hong, and J. A. Madri, Regulation of human colonic cell line proliferation and phenotype by sodium butyrate. Dig. Dis. Sci. 41, 1989 (1996).
26. M. Markowska, R. Oberle, S. Juzwin, C. P. Hsu, M. Gryszkiewicz, and A. J. Streeter, Optimizing Caco-2 cell monolayers to increase throughput in drug intestinal absorption analysis. J. Pharmacol. Toxicol. Methods 46, 51 (2001).
27. J. M. Mariadason, K. L. Rickard, D. H. Barkla, L. H. Augenlicht, and P. R. Gibson, Divergent phenotypic patterns and commitment to apoptosis of Caco-2 cells during spontaneous and butyrate-induced differentiation. J. Cell Physiol. 183, 347 (2000).
28. A. Cerbone, C. Toaldo, S. Laurora, F. Briatore, S. Pizzimenti, M. U. Dianzani, C. Ferretti, and G. Barrera, 4-Hydroxynonenal and PPARgamma ligands affect proliferation, differentiation, and apoptosis in colon cancer cells. Free Radic. Biol. Med. 42, 1661 (2007).
29. P W. Sylvester, Optimization of the tetrazolium dye (MTT) colorimetric assay for cellular growth and viability. Methods Mol. Biol. 716, 157 (2011).
30. S. J. Collins, The HL-60 promyelocytic leukemia cell line: Proliferation, differentiation, and cellular oncogene expression. Blood 70, 1233 (1987).
31. R. D. Curren, G. C. Mun, D. P. Gibson, and M. J. Aardema, Development of a method for assessing micronucleus induction in a 3D human skin model (EpiDerm). Mutat. Res. 607, 192 (2006).
32. S. J. Collins, F. W. Ruscetti, R. E. Gallagher, and R. C. Gallo, Terminal differentiation of human promyelocytic leukemia cells induced by dimethyl sulfoxide and other polar compounds. Proc. Natl. Acad. Sci. U. S. A. 75, 2458 (1978).
33. G. Barrera, C. Di Mauro, R. Muraca, D. Ferrero, G. Cavalli, V. M. Fazio, L. Paradisi, and M. U. Dianzani, Induction of differentiation in human HL-60 cells by 4-hydroxynonenal, a product of lipid peroxidation. Exp. Cell. Res. 197, 148 (1991).
34. D. Bei, J. Meng, and B. B. Youan, Engineering nanomedicines for improved melanoma therapy: Progress and promises. Nanomedicine (Lond) 5, 1385 (2010).
35. V. M. Schoop, N. Mirancea, and N. E. Fusenig, Epidermal organization and differentiation of HaCaT keratinocytes in organotypic coculture with human dermal fibroblasts. J. Invest. Dermatol. 112, 343 (1999).
36. P. C. Baer, J. Bereiter-Hahn, R. Schubert, and H. Geiger, Differentiation status of human renal proximal and distal tubular epithelial cells in vitro: differential expression of characteristic markers. Cells Tissues Organs 184, 16 (2006).
37. S. Kustermann, T. Manigold, C. Ploix, M. Skubatz, T. Heckel, H. Hinton, T. Weiser, T. Singer, L. Suter, and A. Roth, A real-time impedance-based screening assay for drug-induced vascular leakage. Toxicol Sci. 138, 333 (2014).
38. P. Artursson, K. Palm, and K. Luthman, Caco-2 monolayers in experimental and theoretical predictions of drug transport. Adv. Drug Deliv. Rev. 46, 27 (2001).
39. F. Delie and W. Rubas, A human colonic cell line sharing similarities with enterocytes as a model to examine oral absorption: Advantages and limitations of the Caco-2 model. Crit. Rev. Ther. Drug Carrier Syst. 14, 221 (1997).
40. S. Pizzimenti, E. Menegatti, D. Berardi, C. Toaldo, P. Pettazzoni, R. Minelli, B. Giglioni, A. Cerbone, M. U. Dianzani, C. Ferretti, and G. Barrera, 4-hydroxynonenal, a lipid peroxidation product of dietary polyunsaturated fatty acids, has anticarcinogenic properties in colon carcinoma cell lines through the inhibition of telomerase activity. J. Nutr. Biochem. 21, 818 (2010).
41. M. M. Abdel-Mottaleb, D. Neumann, and A. Lamprecht, In vitro drug release mechanism from lipid nanocapsules (LNC). Int. J. Pharm. 390, 208 (2010).
42. S. Pizzimenti, E. Ciamporcero, P. Pettazzoni, S. Osella-Abate, M. Novelli, C. Toaldo, M. Husse, M. Daga, R. Minelli, A. Bisazza, P. Ferruti, E. Ranucci, M. G. Bernengo, C. Dianzani, F. Biasi, R. Cavalli, and G. Barrera, The inclusion complex of 4-hydroxynonenal with a polymeric derivative of beta-cyclodextrin enhances the antitumoral efficacy of the aldehyde in several tumor cell lines and in a three-dimensional human melanoma model. Free Radic. Biol. Med. 65, 765 (2013).
43. F. Gentile, S. Pizzimenti, A. Arcaro, P. Pettazzoni, R. Minelli, D. D'Angelo, G. Mamone, P. Ferranti, C. Toaldo, G. Cetrangolo, S. Formisano, M. U. Dianzani, K. Uchida, C. Dianzani, and G. Barrera, Exposure of HL-60 human leukaemic cells to 4-hydroxynonenal promotes the formation of adduct(s) with alphaenolase devoid of plasminogen binding activity. Biochem. J. 422, 285 (2009).
44. S. Pizzimenti, E. Ciamporcero, M. Daga, P. Pettazzoni, A. Arcaro, G. Cetrangolo, R. Minelli, C. Dianzani, A. Lepore, F. Gentile, and G. Barrera, Interaction of aldehydes derived from lipid peroxidation and membrane proteins. Front Physiol. 4, 242 (2013).
45. B. G. Hill, P. Haberzettl, Y. Ahmed, S. Srivastava, and A. Bhatnagar, Unsaturated lipid peroxidation-derived aldehydes activate autophagy in vascular smooth-muscle cells. Biochem. J. 410, 525 (2008).
46. C. Garbe, T. K. Eigentler, U. Keilholz, A. Hauschild, and J. M. Kirkwood, Systematic review of medical treatment in melanoma: Current status and future prospects. Oncologist 16, 5 (2011).
47. H. Vörsmann, F. Groeber, H. Walles, S. Busch, S. Beissert, H. Walczak, and D. Kulms, Development of a human threedimensional organotypic skin-melanoma spheroid model for in vitro drug testing. Cell Death Dis. 4, e719 (2013).
48. B. M. Baker and C. S. Chen, Deconstructing the third dimension: How 3D culture microenvironments alter cellular cues. J. Cell Sci. 125, 3015 (2012).
49. G. Micali, F. Lacarrubba, M. R. Nasca, S. Ferraro, and R. A. Schwartz, Topical pharmacotherapy for skin cancer: Part II clinical applications. J. Am. Acad. Dermatol. 70, 979-e1-12 (2014).
50. D. C. Hassane, M. L. Guzman, C. Corbett, X. Li, R. Abboud, F. Young, J. Liesveld, M. Carroll, and C. T. Jordan, Discovery of agents that eradicate leukemia stem cells using an in silico screen of public gene expression data. Blood 111, 5654 (2008).
51. T. Semlitsch, H. M. Tillian, N. Zarkovic, S. Borovic, M. Purtscher, O. Hohenwarter, and R. J. Schaur, Differential influence of the lipid peroxidation product 4-hydroxynonenal on the growth of human lymphatic leukaemia cells and human periopherial blood lymphocytes. Anticancer Res. 22, 1689 (2002).
52. S. Pizzimenti, C. Toaldo, P. Pettazzoni, M. U. Dianzani, and G. Barrera, The "two-faced" effects of reactive oxygen species and the lipid peroxidation product 4-hydroxynonenal in the hallmarks of cancer. Cancers 2, 338 (2010).
53. T. P. Szatrowski and C. F. Nathan, Production of large amounts of hydrogen peroxide by human tumor cells. Cancer Res. 51, 794 (1991).
54. S. Kawanishi, Y. Hiraku, S. Pinlaor, and N. Ma, Oxidative and nitrative DNA damage in animals and patients with inflammatory diseases in relation to inflammation-related carcinogenesis. Biol. Chem. 387, 365 (2006).
55. G. Barrera, Oxidative stress and lipid peroxidation products in cancer progression and therapy. ISRN Oncol. 137289 (2012).
56. K. Cal and K. Centkowska, Use of cyclodextrins in topical formulations: Practical aspects. Eur. J. Pharm. Biopharm. 68, 467 (2008).
57. G. Piel, S. Moutard, E. Uhoda, F. Pilard, G. E. Pierard, B. Perly, L. Delattre, and B. Evrard, Skin compatibility of cyclodextrins and their derivatives: A comparative assessment using a corneoxenometry bioassay. Eur. J. Pharm. Biopharm. 57, 479 (2004).