Enzymatic Biodegradation of Hydrogels for Protein Delivery Targeted to the Small Intestine

Biomacromolecules

Volumn 16, Issue 3, 2015, Pages 962-972

  Knipe, Jennifer M ^a   Chen, Frances ^a   Peppas, Nicholas A ^a,b  

^a The University of Texas at Austin   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIODEGRADATION; CATALYSIS; CELL CULTURE; CROSSLINKING; CYTOTOXICITY; DEGRADATION; ENZYMES; GELS; PEPTIDES; PROTEINS;

CARBOXYLIC ACID GROUPS; CYTOTOXIC EFFECTS; DEGRADATION MECHANISM; DEGRADATION PRODUCTS; FUNCTION OF TIME; METHACRYLIC ACIDS; N VINYLPYRROLIDONE; PH-RESPONSIVE SWELLINGS;

HYDROGELS;

CARBOXYLIC ACID; OLIGOPEPTIDE; POLY(METHACRYLIC ACID CO N VINYLPYRROLIDONE); POLYMER; PROTEIN; TRYPSIN; UNCLASSIFIED DRUG; DELAYED RELEASE FORMULATION; HYDROGEL; INSULIN; POLYMETHACRYLIC ACID DERIVATIVE;

ANIMAL EXPERIMENT; ARTICLE; BIODEGRADATION; CONTROLLED STUDY; CROSS LINKING; CYTOTOXICITY; DRUG DELIVERY SYSTEM; HYDROGEL; INFRARED SPECTROSCOPY; NONHUMAN; PH; PRIORITY JOURNAL; RAT; SMALL INTESTINE; SYNTHESIS; TURBIDITY; ANIMAL; BIOCATALYSIS; CELL LINE; CHEMISTRY; DELAYED RELEASE FORMULATION; HUMAN; MOUSE; PROTEIN DEGRADATION;

RATTUS;

ANIMALS; BIOCATALYSIS; CELL LINE; DELAYED-ACTION PREPARATIONS; HUMANS; HYDROGELS; HYDROGEN-ION CONCENTRATION; INSULIN; INTESTINE, SMALL; MICE; OLIGOPEPTIDES; POLYMETHACRYLIC ACIDS; PROTEOLYSIS; RATS; TRYPSIN;

EID: 84924402062     PISSN: 15257797     EISSN: 15264602     Source Type: Journal    
DOI: 10.1021/bm501871a     Document Type: Article

References (63)

1. Peppas, N. A.; Hilt, J. Z.; Khademhosseini, A.; Langer, R. Hydrogels in biology and medicine: from molecular principles to bionanotechnology Adv. Mater. 2006, 18, 1345-1360
2. Hoffman, A. S. Environmentally sensitive polymers and hydrogels MRS Bull. 1991, 16, 42-46
3. Qiu, Y.; Park, K. Envinronment-sensitive hydrogels for drug delivery Adv. Drug Delivery Rev. 2001, 53, 321-339
4. Caldorera-Moore, M.; Peppas, N. A. Micro- and nanotechnologies for intelligent and responsive biomaterial-based medical systems Adv. Drug Delivery Rev. 2009, 61, 1391-1401
5. Bae, H.; Puranik, A. S.; Gauvin, R.; Edalat, F.; Carrillo-Conde, B.; Peppas, N. A.; Khademhosseini, A. Building vascular networks Sci. Transl. Med. 2012, 4, 1-5
6. Phelps, E. A.; Landazuri, N.; Thule, P. M.; Taylor, W. R.; Garcia, A. J. Bioartificial matrices for therapeutic vascularization Proc. Natl. Acad. Sci. U.S.A. 2009, 107, 3323-3328
7. Lin, C.-W.; Tseng, S. J.; Kempson, I. M.; Yang, S.-C.; Hong, T.-M.; Yang, P.-C. Extracellular delivery of modified oligonucleotide and superparamagnetic iron oxide nanoparticles from a degradable hydrogel triggered by tumor acidosis Biomaterials 2013, 34, 4387-4393
8. Liechty, W. B.; Peppas, N. A. Expert opinion: Responsive polymer nanoparticles in cancer therapy Eur. J. Pharm. Biopharm. 2012, 80, 241-246
9. Wong, S.; Shim, M. S.; Kwon, Y. J. Synthetically designed peptide-based biomaterials with stimuli-responsive and membrane-active properties for biomedical applications J. Mater. Chem. B 2014, 2, 595
10. Forbes, D. C.; Peppas, N. A. Polymeric nanocarriers for siRNA delivery to murine macrophages Macromol. Biosci. 2014, 14, 1096-1105
11. Liang, K.; Such, G. K.; Johnston, A. P. R.; Zhu, Z.; Ejima, H.; Richardson, J. J.; Cui, J.; Caruso, F. Endocytic pH-triggered degradation of nanoengineered multilayer capsules Adv. Mater. 2014, 26, 1901-1905
12. Guvendiren, M.; Burdick, J. A. Engineering synthetic hydrogel microenvironments to instruct stem cells Curr. Opin Biotechnol. 2013, 24, 841-846
13. Kirschner, C. M.; Anseth, K. S. Hydrogels in healthcare: from static to dynamic material microenvironments Acta Mater. 2013, 61, 931-944
14. Knipe, J. M.; Peppas, N. A. Multi-responsive hydrogels for drug delivery and tissue engineering applications Regener. Biomater. 2014, 1, 57-65
15. Holzapfel, B. M.; Reichert, J. C.; Schantz, J.-T.; Gbureck, U.; Rackwitz, L.; Nöth, U.; Jakob, F.; Rudert, M.; Groll, J.; Hutmacher, D. W. How smart do biomaterials need to be? A translational science and clinical point of view Adv. Drug Delivery Rev. 2013, 65, 581-603
16. Peppas, N. A.; Bures, P.; Leobandung, W.; Ichikawa, H. Hydrogels in pharmaceutical formulations Eur. J. Pharm. Biopharm. 2000, 50, 27-46
17. Kost, J.; Langer, R. Responsive polymeric delivery systems Adv. Drug Delivery Rev. 2012, 64, 327-341
18. Torres-Lugo, M.; Peppas, N. A. Preparation and characterization of P(MAA-g-EG) nanospheres for protein delivery applications J. Nanopart. Res. 2002, 4, 73-81
19. Torres-Lugo, M.; Peppas, N. A. Molecular design and in vitro studies of novel pH-sensitive hydrogels for the oral delivery of calcitonin Macromolecules 1999, 32, 6646-6651
20. Knipe, J. M.; Chen, F.; Peppas, N. A. Multiresponsive polyanionic microgels with inverse pH responsive behavior by encapsulation of polycationic nanogels J. Appl. Polym. Sci. 2014, 131, 40098
21. Lowman, A. M.; Morishita, M.; Kajita, M.; Nagai, T.; Peppas, D. N. A. Oral delivery of insulin using pH-responsive complexation gels J. Pharm. Sci. 1999, 88, 933-937
22. Carr, D. A.; Peppas, N. A. Assessment of poly(methacrylic acid-co-N-vinyl pyrrolidone) as a carrier for the oral delivery of therapeutic proteins using Caco-2 and HT29-MTX cell lines J. Biomed. Mater. Res., Part A 2009, 92, 504-512
23. Carr, D. A.; Gomez-Burgaz, M.; Boudes, M. C.; Peppas, N. A. Complexation hydrogels for the oral delivery of growth hormone and salmon calcitonin Ind. Eng. Chem. Res. 2010, 49, 11991-11995
24. Hu, J.; Zhang, G.; Liu, S. Enzyme-responsive polymeric assemblies, nanoparticles and hydrogels Chem. Soc. Rev. 2012, 41, 5933
25. Torres, M. P.; Determan, A. S.; Anderson, G. L.; Mallapragada, S. K.; Narasimhan, B. Amphiphilic polyanhydrides for protein stabilization and release Biomaterials 2007, 28, 108-116
26. Lopac, S. K.; Torres, M. P.; Wilson-Welder, J. H.; Wannemuehler, M. J.; Narasimhan, B. Effect of polymer chemistry and fabrication method on protein release and stability from polyanhydride microspheres J. Biomed Mater. Res., Part B 2009, 91, 938-947
27. Thombre, A. G.; Himmelstein, K. J. A simultaneous transport-reaction model for controlled drug delivery from catalyzed bioerodible polymer matrices AIChE J. 1985, 31, 159-766
28. Lao, L. L.; Venkatraman, S. S.; Peppas, N. A. Modeling of drug release from biodegradable polymer blends Eur. J. Pharm. Biopharm. 2008, 70, 796-803
29. Anderson, J. M.; Shive, M. S. Biodegradation and biocompatibility of PLA and PLGA microspheres Adv. Drug Delivery Rev. 2012, 64, 72-82
30. Glangchai, L. C.; Caldorera-Moore, M.; Shi, L.; Roy, K. Nanoimprint lithography based fabrication of shape-specific, enzymatically-triggered smart nanoparticles J. Controlled Release 2008, 125, 263-272
31. Guo, D.-S.; Wang, K.; Wang, Y.-X.; Liu, Y. Cholinesterase-responsive supramolecular vesicle J. Am. Chem. Soc. 2012, 134, 10244-10250
32. Ulbrich, K.; Strohalm, J.; Kopecek, J. Polymers containing enzymatically degradable bonds. VI. Hydrophilic gels cleavable by chymotrypsin Biomaterials 1982, 3, 150-154
33. Subr, V.; Duncan, R.; Kopecek, J. Release of macromolecules from hydrophlilic gels containing enzymatically degradable bonds J. Biomater. Sci., Polym. Ed. 1990, 1, 261-278
34. Vlieghe, P.; Lisowski, V.; Martinez, J.; Khrestchatisky, M. Synthetic therapeutic peptides: science and market Drug Discovery Today 2010, 15, 40-56
35. Wanakule, P.; Liu, G. W.; Fleury, A. T.; Roy, K. Nano-inside-micro: disease-responsive microgels with encapsulated nanoparticles for intracellular drug delivery to the deep lung J. Controlled Release 2012, 162, 429-437
36. Thornton, P. D.; Mart, R. J.; Ulijn, R. V. Enzyme-responsive polymer hydrogel particles for controlled release Adv. Mater. 2007, 19, 1252-1256
37. United States Pharmacopeia; USP 29: The National Formulary; NF 24: Reagents: Test Solutions; United States Pharmacopeial Convention: Rockville, MD, 2006.
38. Yamagata, T.; Morishita, M.; Kavimandan, N. J.; Nakamura, K.; Fukuoka, Y.; Takayama, K.; Peppas, N. A. Characterization of insulin protection properties of complexation hydrogels in gastric and intestinal enzyme fluids J. Controlled Release 2006, 112, 343-349
39. Klinger, D.; Landfester, K. Enzymatic- and light-degradable hybrid nanogels: crosslinking of polyacrylamide with acrylate-functionalized dextrans containing photocleavable linkers J. Polym. Sci., Part A: Polym. Chem. 2012, 50, 1062-1075
40. Yanes, O.; Villanueva, J.; Querol, E.; Aviles, F. Enzymatic measurements for the detection of trypsin and carboxypeptidase A inhibitory activity; http://www.nature.com/protocolexchange/protocols/331.
41. Odian, G. Principles of Polymerization, 4 ed.; Wiley: New York, 2004.
42. Brandup, J.; Immergut, E. H. Polymer Handbook, 3 ed.; Wiley: New York, 1989.
43. Lowman, A. M.; Peppas, N. A. Analysis of the complexation/decomplexation phenomena in graft copolymer networks Macromolecules 1997, 30, 4959-4965
44. Hermanson, G. T. Bioconjugate Techniques; Academic Press, Inc.: San Diego, CA, 1996.
45. Bohlen, P.; Stein, S.; Dairman, W.; Undenfriend, S. Fluorometric assay of proteins in the nanogram range Arch. Biochem. Biophys. 1973, 155, 213-220
46. Kolev, T. Solid-state IR-LD spectroscopic and theoretical analysis of arginine-containing peptides Biopolymers 2006, 83, 39-45
47. Olsen, J. V. Trypsin cleaves exclusively C-terminal to arginine and lysine residues Mol. Cell. Proteomics 2004, 3, 608-614
48. Xu, J.; Ye, J.; Liu, S. Synthesis of well-defined cyclic poly(N-isopropylacrylamide) via click chemistry and its unique thermal phase transition behavior Macromolecules 2007, 40, 9103-9110
49. Qiu, X.-P.; Tanaka, F.; Winnik, F. M. Temperature-induced phase transition of well-defined cyclic poly(N-isopropylacrylamide)s in aqueous solution Macromolecules 2007, 40, 7069-7071
50. Klinger, D.; Landfester, K. Photo-sensitive PMMA microgels: light-triggered swelling and degradation Soft Matter 2011, 7, 1426-1440
51. Lechner, M. D. Influence of Mie scattering on nanoparticles with different particle sizes and shapes: photometry and analytical ultracentrifugation with absorption optics J. Serb. Chem. Soc. 2005, 70, 361-369
52. Cheng, F.; Choy, Y. B.; Choi, H.; Kim, K. Modeling of small-molecule release from crosslinked hydrogel microspheres: effect of crosslinking and enzymatic degradation of hydrogel matrix Int. J. Pharm. 2011, 403, 90-95
53. Peppas, N. A.; Narasimhan, B. Mathematical models in drug delivery: how modeling has shaped the way we design new drug delivery systems J. Controlled Release 2014, 190, 75-81
54. Joshi, A.; Himmelstein, K. J. Dynamics of controlled release from bioerodible matrices J. Controlled Release 1991, 15, 95-104
55. Rice, M. A.; Sanchez-Adams, J.; Anseth, K. S. Exogenously triggered, enzymatic degradation of photopolymerized hydrogels with polycaprolactone subunits: experimental observation and modeling of mass loss behavior Biomacromolecules 2006, 7, 1968-1975
56. Davis, S. S.; Hardy, J. G.; Fara, J. W. Transit of pharmaceutical dosage forms through the small intestine Gut 1986, 27, 886-892
57. Schwert, G. W.; Takenaka, Y. A spectrophotometric determination of trypsin and chymotrypsin Biochim. Biophys. Acta 1955, 16, 570-575
58. Pace, J. LXVIII. The inactivation of trypsin by heat Biochem. J. 1930, 24, i3
59. Kaplan, J. G.; Bona, C. Proteases as mitogens: the effect of trypsin and pronase on mouse and human lymphocytes Exp. Cell Res. 1974, 88, 388-394
60. Unanue, E. R. Antigen-presenting function of the macrophage Annu. Rev. Immunol. 1984, 2, 395-428
61. Kavimandan, N.; Losi, E.; Peppas, N. Novel delivery system based on complexation hydrogels as delivery vehicles for insulin-transferrin conjugates Biomaterials 2006, 27, 3846-3854
62. Peppas, N. A.; Kavimandan, N. J. Nanoscale analysis of protein and peptide absorption: insulin absorption using complexation and pH-sensitive hydrogels as delivery vehicles Eur. J. Pharm. Sci. 2006, 29, 183-197
63. Nakamura, K.; Murray, R. J.; Joseph, J. I.; Peppas, N. A.; Morishita, M.; Lowman, A. M. Oral insulin delivery using P(MAA-g-EG) hydrogels: effects of network morphology on insulin delivery characteristics J. Controlled Release 2004, 95, 589-599