A Combinative Assembly Strategy Inspired Reversibly Borate-Bridged Polymeric Micelles for Lesion-Specific Rapid Release of Anti-Coccidial Drugs
Corresponding Author: Jianping Zhou
Nano-Micro Letters,
Vol. 12 (2020), Article Number: 155
Abstract
Stimuli-triggered drug delivery systems hold vast promise in local infection treatment for the site-specific targeting and shuttling of drugs. Herein, chitosan conjugates (SPCS) installed with sialic acid (SA) and phenylboronic acid (PBA) were synthesized, of which SA served as targeting ligand for coccidium and reversible-binding bridge for PBA. The enhanced drug-loading capacity of SPCS micelles was attributed to a combination assembly from hydrophobicity-driving and reversible borate bridges. The drug-loaded SPCS micelles shared superior biostability in upper gastrointestinal tract. After reaching the lesions, the borate bridges were snipped by carbohydrates under a higher pH followed by accelerated drug release, while SA exposure on micellar surface facilitated drug cellular internalization to eliminate parasites inside. The drug-micelles revealed an enhanced anti-coccidial capacity with a higher index of 185.72 compared with commercial preparation. The dual-responsive combination of physicochemical assembly could provide an efficient strategy for the exploitation of stable, safe and flexible anti-infectious drug delivery systems.
Highlights:
1 A combined assembly strategy from hydrophobicity-driving and reversible borate bridges is proposed for high drug-loading efficiency and superior stability.
2 Intestinal environment-triggered drug delivery system represents an effective treatment for local infection due to the site-specific targeting and shuttling of drugs.
3 The reduced dosage brought by the drug-loading micelles could solve the problem of drug residue in breeding industry.
Keywords
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- M. Wallach, Role of antibody in immunity and control of chicken coccidiosis. Trends Parasitol. 26(8), 382–387 (2010). https://doi.org/10.1016/j.pt.2010.04.004
- B. Gummow, Challenges posed by new and re-emerging infectious diseases in livestock production, wildlife and humans. Livest Sci. 130(1), 41–46 (2010). https://doi.org/10.1016/j.livsci.2010.02.009
- A. Brioudes, J. Warner, R. Hedlefs, B. Gummow, Diseases of livestock in the Pacific Islands region: setting priorities for food animal biosecurity. Acta Trop. 143, 66–76 (2015). https://doi.org/10.1016/j.actatropica.2014.12.012
- D.P. Blake, E.L. Clark, S.E. Macdonald, V. Thenmozhi, K. Kundu et al., Population, genetic, and antigenic diversity of the apicomplexan Eimeria tenella and their relevance to vaccine development. PNAS 112(38), 5343–5350 (2015). https://doi.org/10.1073/pnas.1506468112
- V. Jain, M. Yogavel, H. Kikuchi, Y. Oshima, N. Hariguchi et al., Targeting prolyl-tRNA synthetase to accelerate drug discovery against malaria, leishmaniasis, toxoplasmosis, cryptosporidiosis, and coccidiosis. Structure 25, 1–11 (2017). https://doi.org/10.1016/j.str.2017.07.015
- A.J. Tanweer, N. Chand, U. Saddique, C.A. Bailey, R.U. Khan, Antiparasitic effect of wild rue (Peganum harmala L) against experimentally induced coccidiosis in broiler chicks. Parasitol. Res. 113(8), 2951–2960 (2014). https://doi.org/10.1007/s00436-014-3957-y
- I.Z. Abbas, anti-coccidial drug resistance in fowl coccidia: the state of play revisited. World Poul. Sci. J. 67(2), 337–350 (2011). https://doi.org/10.1017/S004393391100033X
- B.H. Zhou, H.W. Wang, X.Y. Wang, L.F. Zhang, K.Y. Zhang, F.Q. Xue, Eimeria tenella: effects of diclazuril treatment on microneme genes expression in second-generation merozoites and pathological changes of caeca in parasitized chickens. Exp. Parasitol. 125(3), 264–270 (2010). https://doi.org/10.1016/j.exppara.2010.01.022
- M. Piest, J.F.J. Engbersen, Role of boronic acid moieties in poly(amido amine)s for gene delivery. J. Control. Release 155(2), 331–340 (2011). https://doi.org/10.1016/j.jconrel.2011.07.011
- C.D.G. Lux, S. Joshibarr, T. Nguyen, E. Mahmoud, E. Schopf, N. Fomina, A. Almutairi, Biocompatible polymeric nanoparticles degrade and release cargo in response to biologically relevant levels of hydrogen peroxide. J. Am. Chem. Soc. 134(38), 15758–15764 (2012). https://doi.org/10.1021/ja303372u
- M. Seno, K. Yoshida, K. Sato, J. Anzai, pH- and sugar-sensitive multilayer films composed of phenylboronic acid (PBA)-modified poly(allylamine hydrochloride) (PBA-PAH) and poly(vinyl alcohol) (PVA): a significant effect of PBA content on the film stability. Mater. Sci. Eng. C Mater. 62, 474–479 (2016). https://doi.org/10.1016/j.msec.2016.02.005
- P.T. Chou, Y.J. Tseng, S.W. Chou, J.J. Shyue, S.Y. Lin, J.K. Hsiao, A versatile theranostic delivery platform integrating magnetic resonance imaging/computed tomography, pH/cis-diol controlled release and targeted therapy. ACS Nano 10(6), 5809 (2016). https://doi.org/10.1021/acsnano.5b08130
- X. Zhang, K. Achazi, R. Haag, Boronate cross-linked ATP- and pH-responsive nanogels for intracellular delivery of anticancer drugs. Adv. Healthc. Mater. 4(4), 585–592 (2015). https://doi.org/10.1002/adhm.201400550
- B. Yang, H. Jia, X. Wang, S. Chen, X. Zhang, R. Zhuo, J. Feng, Self-assembled vehicle construction via boronic acid coupling and host–guest interaction for serum-tolerant DNA transport and pH-responsive drug delivery. Adv. Healthc. Mater. 3(4), 596–608 (2014). https://doi.org/10.1002/adhm.201300162
- W. Xu, J. Ding, L. Li, C. Xiao, X. Zhuang, X. Chen, Acid-labile boronate-bridged dextran-bortezomib conjugate with up-regulated hypoxic tumor suppression. Chem. Commun. 51(31), 6812–6815 (2015). https://doi.org/10.1039/c5cc01371b
- J. Kim, J. Lee, Y.M. Lee, S. Pramanick, S. Im, W.J. Kim, Andrographolide-loaded polymerized phenylboronic acid nanoconstruct for stimuli-responsive chemotherapy. J. Control. Rel. 259, 203–211 (2016). https://doi.org/10.1016/j.jconrel.2016.10.029
- S. Deshayes, H. Cabral, T. Ishii, Y. Miura, S. Kobayashi et al., Phenylboronic acid-installed polymeric micelles for targeting sialylated epitopes in solid tumors. J. Am. Chem. Soc. 135(41), 15501–15507 (2013). https://doi.org/10.1021/ja406406h
- H. Otsuka, E. Uchimura, H. Koshino, T. Okano, K. Kataoka, Anomalous binding profile of phenylboronic acid with N-acetylneuraminic acid (Neu5Ac) in aqueous solution with varying pH. J. Am. Chem. Soc. 125(12), 3493–3502 (2003). https://doi.org/10.1021/ja021303r
- B.E. Kidd, X. Li, R.C. Piemonte, T.J. Cooksey, A. Singh, M.L. Robertson, L.A. Madsen, Tuning biocompatible block copolymer micelles by varying solvent composition: dynamics and populations of micelles and unimers. Macromolecules 50(11), 4322–4334 (2017). https://doi.org/10.1021/acs.macromol.6b02580
- M.C. Chen, F.L. Mi, Z.X. Liao, C.W. Hsiao, K. Sonaje, M.F. Chung, L.W. Hsu, H.W. Sung, Recent advances in chitosan-based nanoparticles for oral delivery of macromolecules. Adv. Drug Del. Rev. 65(6), 865–879 (2013). https://doi.org/10.1016/j.addr.2012.10.010
- T. Kean, M. Thanou, Biodegradation, biodistribution and toxicity of chitosan. Adv. Drug Del. Rev. 62(1), 3–11 (2010). https://doi.org/10.1016/j.addr.2009.09.004
- S. Swiatkiewicz, M. Swiatkiewicz, A. Arczewska-Wlosek, D. Jozefiak, Chitosan and its oligosaccharide derivatives (chito-oligosaccharides) as feed supplements in poultry and swine nutrition. J. Anim. Physiol. Anim. Nutr. 99(1), 1–12 (2015). https://doi.org/10.1111/jpn.12222
- J.H. Park, G. Saravanakumar, K. Kim, I.C. Kwon, Targeted delivery of low molecular drugs using chitosan and its derivatives. Adv. Drug Del. Rev. 62(1), 28–41 (2010). https://doi.org/10.1016/j.addr.2009.10.003
- D. Zhao, J.Q. Xu, X. Yi, Q. Zhang, S.X. Cheng, R.X. Zhuo, F. Li, A pH-activated targeting drug delivery system based on the selective binding of phenylboronic acid. ACS Appl. Mater. Interfaces 8(23), 14845 (2016). https://doi.org/10.1021/acsami.6b04737
- K. Joseph, L. Robert, Responsive polymeric delivery systems. Adv. Drug Del. Rev. 64(1–3), 327–341 (2012). https://doi.org/10.1016/s0169-409x(00)00136-8
References
M. Wallach, Role of antibody in immunity and control of chicken coccidiosis. Trends Parasitol. 26(8), 382–387 (2010). https://doi.org/10.1016/j.pt.2010.04.004
B. Gummow, Challenges posed by new and re-emerging infectious diseases in livestock production, wildlife and humans. Livest Sci. 130(1), 41–46 (2010). https://doi.org/10.1016/j.livsci.2010.02.009
A. Brioudes, J. Warner, R. Hedlefs, B. Gummow, Diseases of livestock in the Pacific Islands region: setting priorities for food animal biosecurity. Acta Trop. 143, 66–76 (2015). https://doi.org/10.1016/j.actatropica.2014.12.012
D.P. Blake, E.L. Clark, S.E. Macdonald, V. Thenmozhi, K. Kundu et al., Population, genetic, and antigenic diversity of the apicomplexan Eimeria tenella and their relevance to vaccine development. PNAS 112(38), 5343–5350 (2015). https://doi.org/10.1073/pnas.1506468112
V. Jain, M. Yogavel, H. Kikuchi, Y. Oshima, N. Hariguchi et al., Targeting prolyl-tRNA synthetase to accelerate drug discovery against malaria, leishmaniasis, toxoplasmosis, cryptosporidiosis, and coccidiosis. Structure 25, 1–11 (2017). https://doi.org/10.1016/j.str.2017.07.015
A.J. Tanweer, N. Chand, U. Saddique, C.A. Bailey, R.U. Khan, Antiparasitic effect of wild rue (Peganum harmala L) against experimentally induced coccidiosis in broiler chicks. Parasitol. Res. 113(8), 2951–2960 (2014). https://doi.org/10.1007/s00436-014-3957-y
I.Z. Abbas, anti-coccidial drug resistance in fowl coccidia: the state of play revisited. World Poul. Sci. J. 67(2), 337–350 (2011). https://doi.org/10.1017/S004393391100033X
B.H. Zhou, H.W. Wang, X.Y. Wang, L.F. Zhang, K.Y. Zhang, F.Q. Xue, Eimeria tenella: effects of diclazuril treatment on microneme genes expression in second-generation merozoites and pathological changes of caeca in parasitized chickens. Exp. Parasitol. 125(3), 264–270 (2010). https://doi.org/10.1016/j.exppara.2010.01.022
M. Piest, J.F.J. Engbersen, Role of boronic acid moieties in poly(amido amine)s for gene delivery. J. Control. Release 155(2), 331–340 (2011). https://doi.org/10.1016/j.jconrel.2011.07.011
C.D.G. Lux, S. Joshibarr, T. Nguyen, E. Mahmoud, E. Schopf, N. Fomina, A. Almutairi, Biocompatible polymeric nanoparticles degrade and release cargo in response to biologically relevant levels of hydrogen peroxide. J. Am. Chem. Soc. 134(38), 15758–15764 (2012). https://doi.org/10.1021/ja303372u
M. Seno, K. Yoshida, K. Sato, J. Anzai, pH- and sugar-sensitive multilayer films composed of phenylboronic acid (PBA)-modified poly(allylamine hydrochloride) (PBA-PAH) and poly(vinyl alcohol) (PVA): a significant effect of PBA content on the film stability. Mater. Sci. Eng. C Mater. 62, 474–479 (2016). https://doi.org/10.1016/j.msec.2016.02.005
P.T. Chou, Y.J. Tseng, S.W. Chou, J.J. Shyue, S.Y. Lin, J.K. Hsiao, A versatile theranostic delivery platform integrating magnetic resonance imaging/computed tomography, pH/cis-diol controlled release and targeted therapy. ACS Nano 10(6), 5809 (2016). https://doi.org/10.1021/acsnano.5b08130
X. Zhang, K. Achazi, R. Haag, Boronate cross-linked ATP- and pH-responsive nanogels for intracellular delivery of anticancer drugs. Adv. Healthc. Mater. 4(4), 585–592 (2015). https://doi.org/10.1002/adhm.201400550
B. Yang, H. Jia, X. Wang, S. Chen, X. Zhang, R. Zhuo, J. Feng, Self-assembled vehicle construction via boronic acid coupling and host–guest interaction for serum-tolerant DNA transport and pH-responsive drug delivery. Adv. Healthc. Mater. 3(4), 596–608 (2014). https://doi.org/10.1002/adhm.201300162
W. Xu, J. Ding, L. Li, C. Xiao, X. Zhuang, X. Chen, Acid-labile boronate-bridged dextran-bortezomib conjugate with up-regulated hypoxic tumor suppression. Chem. Commun. 51(31), 6812–6815 (2015). https://doi.org/10.1039/c5cc01371b
J. Kim, J. Lee, Y.M. Lee, S. Pramanick, S. Im, W.J. Kim, Andrographolide-loaded polymerized phenylboronic acid nanoconstruct for stimuli-responsive chemotherapy. J. Control. Rel. 259, 203–211 (2016). https://doi.org/10.1016/j.jconrel.2016.10.029
S. Deshayes, H. Cabral, T. Ishii, Y. Miura, S. Kobayashi et al., Phenylboronic acid-installed polymeric micelles for targeting sialylated epitopes in solid tumors. J. Am. Chem. Soc. 135(41), 15501–15507 (2013). https://doi.org/10.1021/ja406406h
H. Otsuka, E. Uchimura, H. Koshino, T. Okano, K. Kataoka, Anomalous binding profile of phenylboronic acid with N-acetylneuraminic acid (Neu5Ac) in aqueous solution with varying pH. J. Am. Chem. Soc. 125(12), 3493–3502 (2003). https://doi.org/10.1021/ja021303r
B.E. Kidd, X. Li, R.C. Piemonte, T.J. Cooksey, A. Singh, M.L. Robertson, L.A. Madsen, Tuning biocompatible block copolymer micelles by varying solvent composition: dynamics and populations of micelles and unimers. Macromolecules 50(11), 4322–4334 (2017). https://doi.org/10.1021/acs.macromol.6b02580
M.C. Chen, F.L. Mi, Z.X. Liao, C.W. Hsiao, K. Sonaje, M.F. Chung, L.W. Hsu, H.W. Sung, Recent advances in chitosan-based nanoparticles for oral delivery of macromolecules. Adv. Drug Del. Rev. 65(6), 865–879 (2013). https://doi.org/10.1016/j.addr.2012.10.010
T. Kean, M. Thanou, Biodegradation, biodistribution and toxicity of chitosan. Adv. Drug Del. Rev. 62(1), 3–11 (2010). https://doi.org/10.1016/j.addr.2009.09.004
S. Swiatkiewicz, M. Swiatkiewicz, A. Arczewska-Wlosek, D. Jozefiak, Chitosan and its oligosaccharide derivatives (chito-oligosaccharides) as feed supplements in poultry and swine nutrition. J. Anim. Physiol. Anim. Nutr. 99(1), 1–12 (2015). https://doi.org/10.1111/jpn.12222
J.H. Park, G. Saravanakumar, K. Kim, I.C. Kwon, Targeted delivery of low molecular drugs using chitosan and its derivatives. Adv. Drug Del. Rev. 62(1), 28–41 (2010). https://doi.org/10.1016/j.addr.2009.10.003
D. Zhao, J.Q. Xu, X. Yi, Q. Zhang, S.X. Cheng, R.X. Zhuo, F. Li, A pH-activated targeting drug delivery system based on the selective binding of phenylboronic acid. ACS Appl. Mater. Interfaces 8(23), 14845 (2016). https://doi.org/10.1021/acsami.6b04737
K. Joseph, L. Robert, Responsive polymeric delivery systems. Adv. Drug Del. Rev. 64(1–3), 327–341 (2012). https://doi.org/10.1016/s0169-409x(00)00136-8