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BioMed Research International
Volume 2013 (2013), Article ID 527418, 13 pages
Biodistribution and Molecular Studies on Orally Administered Nanoparticle-AON Complexes Encapsulated with Alginate Aiming at Inducing Dystrophin Rescue in mdx Mice
1Department of Medical Sciences, University of Ferrara, 44121 Ferrara, Italy
2Unit of Molecular Medicine for Neuromuscular and Neurodegenerative Diseases, Bambino Gesù Children's Hospital, IRCCS, 00146 Rome, Italy
3Department of Biology and Evolution, University of Ferrara, 44121 Ferrara, Italy
4IGM-CNR, Unit of Bologna c/o IOR, 40136 Bologna, Italy
5Department of Biomedical Sciences, University of Padua, 35121 Padua, Italy
6Department of Environmental and Life Sciences INSTM, University of Eastern Piedmont, 15121 Alessandria, Italy
7Department of Medical Sciences, Section of Medical Genetics, University of Ferrara, via Fossato di Mortara 74, 44121 Ferrara, Italy
Received 1 July 2013; Revised 10 October 2013; Accepted 14 October 2013
Academic Editor: Akinori Nakamura
Copyright © 2013 Maria Sofia Falzarano et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
- J. C. van Deutekom, A. A. Janson, I. B. Ginjaar et al., “Local dystrophin restoration with antisense oligonucleotide PRO051,” The New England Journal of Medicine, vol. 357, no. 26, pp. 2677–2686, 2007.
- S. D. Wilton and S. Fletcher, “Exon skipping and Duchenne muscular dystrophy: hope, hype and how feasible?” Neurology India, vol. 56, no. 3, pp. 254–262, 2008.
- G. J. van Ommen, J. van Deutekom, and A. Aartsma-Rus, “The therapeutic potential of antisense-mediated exon skipping,” Current Opinion in Molecular Therapeutics, vol. 10, no. 2, pp. 140–149, 2008.
- N. M. Goemans, M. Tulinius, J. T. van den Akker et al., “Systemic administration of PRO051 in Duchenne's muscular dystrophy,” The New England Journal of Medicine, vol. 364, no. 16, pp. 1513–1522, 2011.
- S. Cirak, V. Arechavala-Gomeza, M. Guglieri et al., “Exon skipping and dystrophin restoration in patients with Duchenne muscular dystrophy after systemic phosphorodiamidate morpholino oligomer treatment: an open-label, phase 2, dose-escalation study,” The Lancet, vol. 378, no. 9791, pp. 595–605, 2011.
- M. Kinali, V. Arechavala-Gomeza, L. Feng et al., “Local restoration of dystrophin expression with the morpholino oligomer AVI-4658 in Duchenne muscular dystrophy: a single-blind, placebo-controlled, dose-escalation, proof-of-concept study,” The Lancet Neurology, vol. 8, no. 10, pp. 918–928, 2009.
- W.-H. Pan and G. A. Clawson, “Antisense applications for biological control,” Journal of Cellular Biochemistry, vol. 98, no. 1, pp. 14–35, 2006.
- C. F. Bennett and E. E. Swayze, “RNA targeting therapeutics: molecular mechanisms of antisense oligonucleotides as a therapeutic platform,” Annual Review of Pharmacology and Toxicology, vol. 50, pp. 259–293, 2010.
- V. Arora, D. C. Knapp, M. T. Reddy, D. D. Weller, and P. L. Iversen, “Bioavailability and efficacy of antisense Morpholino oligomers targeted to c-myc and cytochrome P-450 3A2 following oral administration in rats,” Journal of Pharmaceutical Sciences, vol. 91, no. 4, pp. 1009–1018, 2002.
- C. J. Mann, K. Honeyman, A. J. Cheng et al., “Antisense-induced exon skipping and synthesis of dystrophin in the mdx mouse,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 1, pp. 42–47, 2001.
- P. Rimessi, P. Sabatelli, M. Fabris et al., “Cationic PMMA nanoparticles bind and deliver antisense oligoribonucleotides allowing restoration of dystrophin expression in the mdx mouse,” Molecular Therapy, vol. 17, no. 5, pp. 820–827, 2009.
- A. Ferlini, P. Sabatelli, M. Fabris et al., “Dystrophin restoration in skeletal, heart and skin arrector pili smooth muscle of mdx mice by ZM2 NP-AON complexes,” Gene Therapy, vol. 17, no. 3, pp. 432–438, 2010.
- E. Bassi, S. Falzarano, M. Fabris, et al., “Persistent dystrophin protein restoration 90 days after a course of intraperitoneally administered naked 2′ OMePS AON and ZM2 NP-AON complexes in mdx mice,” Journal of Biomedicine and Biotechnology, vol. 2012, Article ID 897076, 8 pages, 2012.
- P. Sicinski, Y. Geng, A. S. Ryder-Cook, E. A. Barnard, M. G. Darlison, and P. J. Barnard, “The molecular basis of muscular dystrophy in the mdx mouse: a point mutation,” Science, vol. 244, no. 4912, pp. 1578–1580, 1989.
- E. P. Hoffman, R. H. Brown Jr., and L. M. Kunkel, “Dystrophin: the protein product of the Duchenne muscular dystrophy locus,” Cell, vol. 51, no. 6, pp. 919–928, 1987.
- E. P. Hoffman, J. E. Morgan, S. C. Watkins, and T. A. Partridge, “Somatic reversion/suppression of the mouse mdx phenotype in vivo,” Journal of the Neurological Sciences, vol. 99, no. 1, pp. 9–25, 1990.
- L. L. Qi, A. Rabinowitz, Y. C. Chen et al., “Systemic delivery of antisense oligoribonucleotide restorers dystrophin expression in body-wide skeletal muscles,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 1, pp. 198–203, 2005.
- J. Xu, S. Ganesh, and M. Amiji, “Non-condensing polymeric nanoparticles for targeted gene and siRNA delivery,” International Journal of Pharmaceutics, vol. 427, no. 1, pp. 21–34, 2012.
- S. Akhtar, “Oral delivery of siRNA and antisense oligonucleotides,” Journal of Drug Targeting, vol. 17, no. 7, pp. 491–495, 2009.
- A. A. Raoof, P. Chiu, Z. Ramtoola et al., “Oral bioavailability and multiple dose tolerability of an antisense oligonucleotide tablet formulated with sodium caprate,” Journal of Pharmaceutical Sciences, vol. 93, no. 6, pp. 1431–1439, 2004.
- R. S. Geary, O. Khatsenko, K. Bunker et al., “Absolute bioavailability of 2′-O-(2-methoxyethyl)-modified antisense oligonucleotides following intraduodenal instillation in rats,” Journal of Pharmacology and Experimental Therapeutics, vol. 296, no. 3, pp. 898–904, 2001.
- A. des Rieux, V. Fievez, M. Garinot, Y.-J. Schneider, and V. Préat, “Nanoparticles as potential oral delivery systems of proteins and vaccines: a mechanistic approach,” Journal of Controlled Release, vol. 116, no. 1, pp. 1–27, 2006.
- S. Maher, T. W. Leonard, J. Jacobsen, and D. J. Brayden, “Safety and efficacy of sodium caprate in promoting oral drug absorption: from in vitro to the clinic,” Advanced Drug Delivery Reviews, vol. 61, no. 15, pp. 1427–1449, 2009.
- L. G. Tillman, R. S. Geary, and G. E. Hardee, “Oral delivery of antisense oligonucleotides in man,” Journal of Pharmaceutical Sciences, vol. 97, no. 1, pp. 225–236, 2008.
- L. Yin, J. Ding, J. Zhang, C. He, C. Tang, and C. Yin, “Polymer integrity related absorption mechanism of superporous hydrogel containing interpenetrating polymer networks for oral delivery of insulin,” Biomaterials, vol. 31, no. 12, pp. 3347–3356, 2010.
- R. M. Samstein, K. Perica, F. Balderrama, M. Look, and T. M. Fahmy, “The use of deoxycholic acid to enhance the oral bioavailability of biodegradable nanoparticles,” Biomaterials, vol. 29, no. 6, pp. 703–708, 2008.
- N. J. Kavimandan, E. Losi, and N. A. Peppas, “Novel delivery system based on complexation hydrogels as delivery vehicles for insulin-transferrin conjugates,” Biomaterials, vol. 27, no. 20, pp. 3846–3854, 2006.
- Z. S. Haidar, R. C. Hamdy, and M. Tabrizian, “Protein release kinetics for core-shell hybrid nanoparticles based on the layer-by-layer assembly of alginate and chitosan on liposomes,” Biomaterials, vol. 29, no. 9, pp. 1207–1215, 2008.
- F. Tuğcu-Demiröz, F. Acartürk, S. Takka, and O. Konuş-Boyunağa, “Evaluation of alginate based mesalazine tablets for intestinal drug delivery,” European Journal of Pharmaceutics and Biopharmaceutics, vol. 67, pp. 491–497, 2007.
- P. V. Finotelli, D. da Silva, M. Sola-Penna et al., “Microcapsules of alginate/chitosan containing magnetic nanoparticles for controlled release of insulin,” Colloids and Surfaces B, vol. 81, no. 1, pp. 206–211, 2010.
- M. George and T. E. Abraham, “Polyionic hydrocolloids for the intestinal delivery of protein drugs: alginate and chitosan—a review,” Journal of Controlled Release, vol. 114, no. 1, pp. 1–14, 2006.
- Y.-H. Lin, H.-F. Liang, C.-K. Chung, M.-C. Chen, and H.-W. Sung, “Physically crosslinked alginate/N,O-carboxymethyl chitosan hydrogels with calcium for oral delivery of protein drugs,” Biomaterials, vol. 26, no. 14, pp. 2105–2113, 2005.
- P. Spitali, P. Rimessi, M. Fabris et al., “Exon skipping-mediated dystrophin reading frame restoration for small mutations,” Human Mutation, vol. 30, no. 11, pp. 1527–1534, 2009.
- C. A. Sewry, “Immunocytochemical analysis of human muscular dystrophy,” Microscopy Research and Technique, vol. 48, no. 3-4, pp. 142–154, 2000.
- Y. Takeshima, M. Yagi, H. Wada et al., “Intravenous infusion of an antisense oligonucleotide results in exon skipping in muscle dystrophin mRNA of Duchenne muscular dystrophy,” Pediatric Research, vol. 59, no. 5, pp. 690–694, 2006.
- H. Heemskerk, C. de Winter, P. van Kuik et al., “Preclinical PK and PD studies on 2′-O-methyl-phosphorothioate RNA antisense oligonucleotides in the mdx mouse model,” Molecular Therapy, vol. 18, no. 6, pp. 1210–1217, 2010.
- H. A. Heemskerk, C. L. de Winter, S. J. de Kimpe et al., “In vivo comparison of 2′-O-methyl phosphorothioate and morpholino antisense oligonucleotides for Duchenne muscular dystrophy exon skipping,” Journal of Gene Medicine, vol. 11, no. 3, pp. 257–266, 2009.
- T. Yokota, Q.-L. Lu, T. Partridge et al., “Efficacy of systemic morpholino exon-skipping in duchenne dystrophy dogs,” Annals of Neurology, vol. 65, no. 6, pp. 667–676, 2009.
- H. H. Tønnesen and J. Karlsen, “Alginate in drug delivery systems,” Drug Development and Industrial Pharmacy, vol. 28, pp. 621–630, 2002.
- R. Pandey and G. K. Khuller, “Chemotherapeutic potential of alginate-chitosan microspheres as anti-tubercular drug carriers,” Journal of Antimicrobial Chemotherapy, vol. 53, no. 4, pp. 635–640, 2004.
- Z. Ahmad, R. Pandey, S. Sharma, and G. K. Khuller, “Pharmacokinetic and pharmacodynamic behaviour of antitubercular drugs encapsulated in alginate nanoparticles at two doses,” International Journal of Antimicrobial Agents, vol. 27, no. 5, pp. 409–416, 2006.
- B. Thu, P. Bruheim, T. Espevik, O. Smidsrød, P. Soon-Shiong, and G. Skjåk-Bræk, “Alginate polycation microcapsules: I. Interaction between alginate and polycation,” Biomaterials, vol. 17, no. 10, pp. 1031–1040, 1996.
- W. R. Gombotz and S. F. Wee, “Protein release from alginate matrices,” Advanced Drug Delivery Reviews, vol. 31, no. 3, pp. 267–285, 1998.
- M. González Ferreiro, L. G. Tillman, G. Hardee, and R. Bodmeier, “Alginate/poly-L-lysine microparticles for the intestinal delivery of antisense oligonucleotides,” Pharmaceutical Research, vol. 19, no. 6, pp. 755–764, 2002.
- O. Borges, J. Tavares, A. de Sousa, G. Borchard, H. E. Junginger, and A. Cordeiro-da-Silva, “Evaluation of the immune response following a short oral vaccination schedule with hepatitis B antigen encapsulated into alginate-coated chitosan nanoparticles,” European Journal of Pharmaceutical Sciences, vol. 32, no. 4-5, pp. 278–290, 2007.
- J.-Y. Tian, X.-Q. Sun, and X.-G. Chen, “Formation and oral administration of alginate microspheres loaded with pDNA coding for lymphocystis disease virus (LCDV) to Japanese flounder,” Fish and Shellfish Immunology, vol. 24, no. 5, pp. 592–599, 2008.
- Y. Zhang, W. Wei, P. Lv, L. Wang, and G. Ma, “Preparation and evaluation of alginate-chitosan microspheres for oral delivery of insulin,” European Journal of Pharmaceutics and Biopharmaceutics, vol. 77, no. 1, pp. 11–19, 2011.
- H. Laroui, G. Dalmasso, H. T. T. Nguyen, Y. Yan, S. V. Sitaraman, and D. Merlin, “Drug-loaded nanoparticles targeted to the colon with polysaccharide hydrogel reduce colitis in a mouse model,” Gastroenterology, vol. 138, no. 3, pp. 843–853, 2010.
- A. I. de las Heras, S. Rodríguez Saint-Jean, and S. I. Pérez-Prieto, “Immunogenic and protective effects of an oral DNA vaccine against infectious pancreatic necrosis virus in fish,” Fish and Shellfish Immunology, vol. 28, no. 4, pp. 562–570, 2010.
- M.-G. Vannucchi, C. Zardo, L. Corsani, and M.-S. Faussone-Pellegrini, “Interstitial cells of Cajal, enteric neurons, and smooth muscle and myoid cells of the murine gastrointestinal tract express full-length dystrophin,” Histochemistry and Cell Biology, vol. 118, no. 6, pp. 449–457, 2002.
- A. Ferlini and P. Rimessi, “Exon skipping quantification by real-time PCR,” Methods in Molecular Biology, vol. 867, pp. 189–199, 2012.