Covalent Incorporation of Trehalose within Hydrogels for Enhanced Long‐Term Functional Stability and Controlled Release of Biomacromolecules

Advanced Healthcare MaterialsVolume 4, Issue 12 p. 1802-1812 Communication Covalent Incorporation of Trehalose within Hydrogels for Enhanced Long-Term Functional Stability and Controlled Release of Biomacromolecules Timothy M. O'Shea, Timothy M. O'Shea Harvard–Massachusetts Institute of Technology Division of Health Sciences and Technology, Institute for Medical Engineering and Science, Massachusetts Institute of Technology, Cambridge, MA, 02139 USA David H. Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, 02139 USASearch for more papers by this authorMatthew J. Webber, Matthew J. Webber David H. Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, 02139 USA Department of Anesthesiology, Children's Hospital Boston, 300 Longwood Avenue, Boston, MA, 02115 USASearch for more papers by this authorAlex A. Aimetti, Alex A. Aimetti InVivo Therapeutics Corporation, One Kendall Square Building 1400 East, Floor 4, Cambridge, MA, 02139 USASearch for more papers by this authorRobert Langer, Corresponding Author Robert Langer Harvard–Massachusetts Institute of Technology Division of Health Sciences and Technology, Institute for Medical Engineering and Science, Massachusetts Institute of Technology, Cambridge, MA, 02139 USA David H. Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, 02139 USA Department of Chemical Engineering, Massachusetts Institute of Technology, Cambridge, MA, 02139 USAE-mail: [email protected]Search for more papers by this author Timothy M. O'Shea, Timothy M. O'Shea Harvard–Massachusetts Institute of Technology Division of Health Sciences and Technology, Institute for Medical Engineering and Science, Massachusetts Institute of Technology, Cambridge, MA, 02139 USA David H. Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, 02139 USASearch for more papers by this authorMatthew J. Webber, Matthew J. Webber David H. Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, 02139 USA Department of Anesthesiology, Children's Hospital Boston, 300 Longwood Avenue, Boston, MA, 02115 USASearch for more papers by this authorAlex A. Aimetti, Alex A. Aimetti InVivo Therapeutics Corporation, One Kendall Square Building 1400 East, Floor 4, Cambridge, MA, 02139 USASearch for more papers by this authorRobert Langer, Corresponding Author Robert Langer Harvard–Massachusetts Institute of Technology Division of Health Sciences and Technology, Institute for Medical Engineering and Science, Massachusetts Institute of Technology, Cambridge, MA, 02139 USA David H. Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, 02139 USA Department of Chemical Engineering, Massachusetts Institute of Technology, Cambridge, MA, 02139 USAE-mail: [email protected]Search for more papers by this author First published: 18 June 2015 https://doi.org/10.1002/adhm.201500334Citations: 19Read the full textAboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onEmailFacebookTwitterLinkedInRedditWechat Graphical Abstract Hydrogels with covalently incorporated trehalose are synthesized using thiol-ene Michael addition. Trehalose hydrogels afford prolonged stabilization and ­controlled release of model enzymes in vitro and in vivo as well as preservation of protein stability under heat and ­lyophilization stressors. Strong and ­ordered hydrogen bonding interactions within covalently incorporated trehalose hydrogels represent a possible mechanism for protein stabilization. Supporting Information As a service to our authors and readers, this journal provides supporting information supplied by the authors. Such materials are peer reviewed and may be re-organized for online delivery, but are not copy-edited or typeset. Technical support issues arising from supporting information (other than missing files) should be addressed to the authors. Filename Description adhm201500334-sup-0001-S1.pdf1.2 MB Supplementary Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article. References 1A. A. Kaspar, J. M. Reichert, Drug Discovery Today 2013, 18, 807. 2A. M. Scott, J. D. Wolchok, L. J. Old, Nat. Rev. Cancer 2012, 12, 278. 3M. S. Kariolis, S. Kapur, J. R. Cochran, Curr. Opin. Biotechnol. 2013, 24, 1072. 4P. J. Carter, Exp. Cell Res. 2011, 317, 1261. 5B. Leader, Q. J. Baca, D. E. Golan, Nat. Rev. Drug Discovery 2008, 7, 21. 6S. Frokjaer, D. E. Otzen, Nat. Rev. Drug Discovery 2005, 4, 298. 7J. M. Reichert, Nat. Rev. Drug Discovery 2003, 2, 695. 8C.-C. Lin, K. Anseth, Pharm. Res. 2009, 26, 631. 9T. Vermonden, R. Censi, W. E. Hennink, Chem. Rev. 2012, 112, 2853. 10R. Langer, Science 1990, 249, 1527. 11R. Censi, P. Di Martino, T. Vermonden, W. E. Hennink, J. Controlled Release 2012, 161, 680. 12T. M. O'Shea, A. A. Aimetti, E. Kim, V. Yesilyurt, R. Langer, Adv. Mater. 2015, 27, 65. 13S. Ramakrishna, Y.-H. Kim, H. Kim, PLoS One 2013, 8, e54282. 14N. J. Tester, A. H. Plaas, D. R. Howland, J. Neurosci. Res. 2007, 85, 1110. 15W. Jiskoot, T. W. Randolph, D. B. Volkin, C. R. Middaugh, C. Schöneich, G. Winter, W. Friess, D. J. A. Crommelin, J. F. Carpenter, J. Pharm. Sci. 2012, 101, 946. 16C.-C. Lin, S. M. Sawicki, A. T. Metters, Biomacromolecules 2007, 9, 75. 17J. D. McCall, K. S. Anseth, Biomacromolecules 2012, 13, 2410. 18P. van de Wetering, A. T. Metters, R. G. Schoenmakers, J. A. Hubbell, J. Controlled Release 2005, 102, 619. 19N. Hammer, F. P. Brandl, S. Kirchhof, V. Messmann, A. M. Goepferich, Macromol. Biosci. 2015, 15, 405. 20S.-C. Chen, Y.-C. Wu, F.-L. Mi, Y.-H. Lin, L.-C. Yu, H.-W. Sung, J. Controlled Release 2004, 96, 285. 21S. Koutsopoulos, L. D. Unsworth, Y. Nagai, S. Zhang, Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 4623. 22C. Pérez, I. J. Castellanos, H. R. Costantino, W. Al-Azzam, K. Griebenow, J. Pharm. Pharmacol. 2002, 54, 301. 23H. Lee, R. J. McKeon, R. V. Bellamkonda, Proc. Natl. Acad. Sci. U.S.A. 2009, 107, 3340. 24J. C. Stanwick, M. D. Baumann, M. S. Shoichet, J. Controlled Release 2012, 160, 666. 25P. V. Iyer, L. Ananthanarayan, Process Biochem. 2008, 43, 1019. 26K. Fu, A. M. Klibanov, R. Langer, Nat. Biotechnol. 2000, 18, 24. 27N. K. Jain, I. Roy, Curr. Protoc. Protein Sci. 2010, 59, 4.9.1. 28J. K. Kaushik, R. Bhat, J. Biol. Chem. 2003, 278, 26458. 29G. John, G. Zhu, J. Li, J. S. Dordick, Angew. Chem. Int. Ed. 2006, 45, 4772. 30H. Taguchi, H. Sunayama, E. Takano, Y. Kitayama, T. Takeuchi, Analyst 2015, 140, 1448. 31L. Mao, S. Luo, Q. Huang, J. Lu, Sci. Rep. 2013, 3, 3126. 32N. C. Veitch, Phytochemistry 2004, 65, 249. 33K. Szigeti, L. Smeller, S. Osváth, Z. Majer, J. Fidy, Biochim. Biophys. Acta 2008, 1784, 1965. 34L. Hassani, B. Ranjbar, K. Khajeh, H. Naderi-Manesh, M. Naderi-Manesh, M. Sadeghi, Enzyme Microb. Technol. 2006, 38, 118. 35R. J. Mancini, J. Lee, H. D. Maynard, J. Am. Chem. Soc. 2012, 134, 8474. 36J. Lee, E.-W. Lin, U. Y. Lau, J. L. Hedrick, E. Bat, H. D. Maynard, Biomacromolecules 2013, 14, 2561. 37E. Bat, J. Lee, U. Y. Lau, H. D. Maynard, Nat. Commun. 2015, 6, 6654. 38K. Chattopadhyay, S. Mazumdar, Biochemistry 2000, 39, 263. 39L. Fu, J. Liu, E. C. Y. Yan, J. Am. Chem. Soc. 2011, 133, 8094. 40B. Schuler, H. Hofmann, Curr. Opin. Struct. Biol. 2013, 23, 36. 41M. A. Singer, S. Lindquist, Mol. Cell 1998, 1, 639. 42K. Imamura, K.-i. Ohyama, T. Yokoyama, Y. Maruyama, H. Imanaka, K. Nakanishi, J. Pharm. Sci. 2008, 97, 519. 43L. S. Taylor, G. Zografi, J. Pharm. Sci. 1998, 87, 1615. 44W. F. Wolkers, A. E. Oliver, F. Tablin, J. H. Crowe, Carbohydr. Res. 2004, 339, 1077. 45M. Roussenova, M. Murith, A. Alam, J. Ubbink, Biomacromolecules 2010, 11, 3237. 46M. Roussenova, J.-C. Andrieux, M. A. Alam, J. Ubbink, Carbohydr. Polym. 2014, 102, 566. 47T. T. Wyatt, M. R. van Leeuwen, E. A. Golovina, F. A. Hoekstra, E. J. Kuenstner, E. A. Palumbo, N. L. Snyder, C. Visagie, A. Verkennis, J. E. Hallsworth, H. A. B. Wösten, J. Dijksterhuis, Environ. Microbiol. 2015, 17, 395. 48N. K. Jain, I. Roy, Protein Sci. 2009, 18, 24. 49M. W. Tibbitt, A. M. Kloxin, L. A. Sawicki, K. S. Anseth, Macromole­cules 2013, 46, 2785. Citing Literature Volume4, Issue12August 26, 2015Pages 1802-1812 ReferencesRelatedInformation