pH-Universal Catechol-Amine Chemistry for Versatile Hyaluronic Acid Bioadhesives
Soohwan An
Department of Biotechnology, Yonsei University, Seoul, 03722 Republic of Korea
Search for more papers by this authorEun Je Jeon
Department of Biotechnology, Yonsei University, Seoul, 03722 Republic of Korea
CellArtgen Inc., Seoul, 03722 Republic of Korea
Search for more papers by this authorSeung Yeop Han
Department of Biotechnology, Yonsei University, Seoul, 03722 Republic of Korea
Search for more papers by this authorJihoon Jeon
Department of Biotechnology, Yonsei University, Seoul, 03722 Republic of Korea
Search for more papers by this authorMi Jeong Lee
Department of Biotechnology, Yonsei University, Seoul, 03722 Republic of Korea
Search for more papers by this authorSooyeon Kim
Department of Biotechnology, Yonsei University, Seoul, 03722 Republic of Korea
Search for more papers by this authorMikyung Shin
Department of Biomedical Engineering, Sungkyunkwan University (SKKU), Suwon, 16419 Republic of Korea
Department of Intelligent Precision Healthcare Convergence, Sungkyunkwan University (SKKU), Suwon, 16419 Republic of Korea
Search for more papers by this authorCorresponding Author
Seung-Woo Cho
Department of Biotechnology, Yonsei University, Seoul, 03722 Republic of Korea
CellArtgen Inc., Seoul, 03722 Republic of Korea
Center for Nanomedicine, Institute for Basic Science (IBS), Seoul, 03722 Republic of Korea
Graduate Program of Nano Biomedical Engineering (NanoBME), Advanced Science Institute, Yonsei University, Seoul, 03722 Republic of Korea
E-mail: [email protected]
Search for more papers by this authorSoohwan An
Department of Biotechnology, Yonsei University, Seoul, 03722 Republic of Korea
Search for more papers by this authorEun Je Jeon
Department of Biotechnology, Yonsei University, Seoul, 03722 Republic of Korea
CellArtgen Inc., Seoul, 03722 Republic of Korea
Search for more papers by this authorSeung Yeop Han
Department of Biotechnology, Yonsei University, Seoul, 03722 Republic of Korea
Search for more papers by this authorJihoon Jeon
Department of Biotechnology, Yonsei University, Seoul, 03722 Republic of Korea
Search for more papers by this authorMi Jeong Lee
Department of Biotechnology, Yonsei University, Seoul, 03722 Republic of Korea
Search for more papers by this authorSooyeon Kim
Department of Biotechnology, Yonsei University, Seoul, 03722 Republic of Korea
Search for more papers by this authorMikyung Shin
Department of Biomedical Engineering, Sungkyunkwan University (SKKU), Suwon, 16419 Republic of Korea
Department of Intelligent Precision Healthcare Convergence, Sungkyunkwan University (SKKU), Suwon, 16419 Republic of Korea
Search for more papers by this authorCorresponding Author
Seung-Woo Cho
Department of Biotechnology, Yonsei University, Seoul, 03722 Republic of Korea
CellArtgen Inc., Seoul, 03722 Republic of Korea
Center for Nanomedicine, Institute for Basic Science (IBS), Seoul, 03722 Republic of Korea
Graduate Program of Nano Biomedical Engineering (NanoBME), Advanced Science Institute, Yonsei University, Seoul, 03722 Republic of Korea
E-mail: [email protected]
Search for more papers by this authorAbstract
Catechol, a major mussel-inspired underwater adhesive moiety, has been used to develop functional adhesive hydrogels for biomedical applications. However, oxidative catechol chemistry for interpolymer crosslinking and adhesion is exclusively effective under alkaline conditions, with limited applications in non-alkaline conditions. To overcome this limitation, pH-universal catechol–amine chemistry to recapitulate naturally occurring biochemical events induced by pH variation in the mussel foot is suggested. Aldehyde moieties are introduced to hyaluronic acid (HA) by partial oxidation, which enables dual-mode catechol tethering to the HA via both stable amide and reactive secondary amine bonds. Because of the presence of additional reactive amine groups, the resultant aldehyde-modified HA conjugated with catechol (AH-CA) is effectively crosslinked in acidic and neutral pH conditions. The AH-CA hydrogel exhibits not only fast gelation via active crosslinking regardless of pH conditions, but also strong adhesion and excellent biocompatibility. The hydrogel enables rapid and robust wound sealing and hemostasis in neutral and alkaline conditions. The hydrogel also mediates effective therapeutic stem cell and drug delivery even in dynamic and harsh environments, such as a motile heart and acidic stomach. Therefore, the AH-CA hydrogel can serve as a versatile biomaterial in a wide range of pH conditions in vivo.
Conflict of Interest
S.-W.C. is a chief technology officer (CTO) of CellArtgen, Inc., Republic of Korea. S.A., E.J.J., and S.-W.C. are co-inventors on a Korean Patent Application (10-2022-0033370) related to the AH-CA hydrogel used in the manuscript.
Open Research
Data Availability Statement
The data that support the findings of this study are available from the corresponding author upon reasonable request.
Supporting Information
Filename | Description |
---|---|
smll202202729-sup-0001-SuppMat.pdf1.7 MB | Supporting Information |
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
- 1C. Zhang, B. Wu, Y. Zhou, F. Zhou, W. Liu, Z. Wang, Chem. Soc. Rev. 2020, 49, 3605.
- 2L. Li, W. Smitthipong, H. Zeng, Polym. Chem. 2015, 6, 353.
- 3H. Lee, S. M. Dellatore, W. M. Miller, P. B. Messersmith, Science 2007, 318, 426.
- 4C. Xie, X. Wang, H. He, Y. Ding, X. Lu, Adv. Funct. Mater. 2020, 30, 1909954.
- 5Y. Li, J. Cheng, P. Delparastan, H. Wang, S. J. Sigg, K. G. DeFrates, Y. Cao, P. B. Messersmith, Nat. Commun. 2020, 11, 3895.
- 6W. Zhang, R. Wang, Z. Sun, X. Zhu, Q. Zhao, T. Zhang, A. Cholewinski, F. K. Yang, B. Zhao, R. Pinnaratip, Chem. Soc. Rev. 2020, 49, 433.
- 7H.-J. Park, Y. Jin, J. Shin, K. Yang, C. Lee, H. S. Yang, S.-W. Cho, Biomacromolecules 2016, 17, 1939.
- 8P. Zhao, K. Wei, Q. Feng, H. Chen, D. S. H. Wong, X. Chen, C.-C. Wu, L. Bian, Chem. Commun. 2017, 53, 12000.
- 9Y. Liu, H. Meng, Z. Qian, N. Fan, W. Choi, F. Zhao, B. P. Lee, Angew. Chem., Int. Ed. 2017, 56, 4224.
- 10K. Zhang, Z. Wei, X. Xu, Q. Feng, J. Xu, L. Bian, Mater. Sci. Eng. C 2019, 103, 109835.
- 11M. Cencer, Y. Liu, A. Winter, M. Murley, H. Meng, B. P. Lee, Biomacromolecules 2014, 15, 2861.
- 12N. Holten-Andersen, M. J. Harrington, H. Birkedal, B. P. Lee, P. B. Messersmith, K. Y. C. Lee, J. H. Waite, Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 2651.
- 13B. K. Ahn, J. Am. Chem. Soc. 2017, 139, 10166.
- 14B. Yang, S. Jin, Y. Park, Y. M. Jung, H. J. Cha, Small 2018, 14, 1803377.
- 15J. H. Waite, J. Exp. Biol. 2017, 220, 517.
- 16G. P. Maier, M. V. Rapp, J. H. Waite, J. N. Israelachvili, A. Butler, Science 2015, 349, 628.
- 17H. Lee, N. F. Scherer, P. B. Messersmith, Proc. Natl. Acad. Sci. USA 2006, 103, 12999.
- 18X. Yang, L. Yuan, Y. Zhao, L. Yan, Y. Bai, J. Ma, S. Li, P. Sorokin, L. Shao, J. Membr. Sci. 2020, 612, 118471.
- 19D. E. Fullenkamp, L. He, D. G. Barrett, W. R. Burghardt, P. B. Messersmith, Macromolecules 2013, 46, 1167.
- 20K. Kim, K. Kim, J. H. Ryu, H. Lee, Biomaterials 2015, 52, 161.
- 21R. Wang, J. Li, W. Chen, T. Xu, S. Yun, Z. Xu, Z. Xu, T. Sato, B. Chi, H. Xu, Adv. Funct. Mater. 2017, 27, 1604894.
- 22C. Kim, Y. Lee, S. H. Lee, J. S. Kim, J. H. Jeong, T. G. Park, Macromol. Res. 2011, 19, 166.
- 23V. Kafil, Y. Omidi, BioImpacts 2011, 1, 23.
- 24S. Choksakulnimitr, S. Masuda, H. Tokuda, Y. Takakura, M. Hashida, J. Controlled Release 1995, 34, 233.
- 25C.-H. Ahn, S. Y. Chae, Y. H. Bae, S. W. Kim, J. Controlled Release 2004, 97, 567.
- 26M. Huang, E. Khor, L.-Y. Lim, Pharm. Res. 2004, 21, 344.
- 27S. An, S. Choi, S. Min, S.-W. Cho, Biotechnol. Bioprocess Eng. 2021, 26, 503.
- 28S. Kim, M. Shin, Tissue Eng. Regener. Med. 2021, 19, 281.
- 29X. Xu, X. Xia, K. Zhang, A. Rai, Z. Li, P. Zhao, K. Wei, L. Zou, B. Yang, W.-K. Wong, Sci. Transl. Med. 2020, 12, eaba8014.
- 30S. A. Svarovsky, R. H. Simoyi, S. V. Makarov, J. Phys. Chem. B 2001, 105, 12634.
- 31P. B. Smith, C. Crespi, Biochem. Pharmacol. 2002, 63, 1941.
- 32S. H. Dieke, C. P. Richter, J. Pharmacol. Exp. Ther. 1945, 83, 195.
- 33M. Li, G. Pan, H. Zhang, B. Guo, J. Polym. Sci. 2022, 60, 1328.
- 34J. Shin, J. S. Lee, C. Lee, H. J. Park, K. Yang, Y. Jin, J. H. Ryu, K. S. Hong, S. H. Moon, H. M. Chung, Adv. Funct. Mater. 2015, 25, 3814.
- 35D. Bermejo-Velasco, S. Kadekar, M. V. Tavares da Costa, O. P. Oommen, K. Gamstedt, J. n. Hilborn, O. P. Varghese, ACS Appl. Mater. Interfaces 2019, 11, 38232.
- 36S. Hong, J. Kim, Y. S. Na, J. Park, S. Kim, K. Singha, G. I. Im, D. K. Han, W. J. Kim, H. Lee, Angew. Chem. 2013, 125, 9357.
10.1002/ange.201301646 Google Scholar
- 37L. Gan, N. C. Tan, A. Gupta, M. Singh, O. Pokholenko, A. Ghosh, Z. Zhang, S. Li, T. W. Steele, Chem. Commun. 2019, 55, 10076.
- 38J.-D. Yang, J. Xue, J.-P. Cheng, Chem. Soc. Rev. 2019, 48, 2913.
- 39J. H. Ryu, Y. Lee, W. H. Kong, T. G. Kim, T. G. Park, H. Lee, Biomacromolecules 2011, 12, 2653.
- 40A. Patgiri, M. Z. Menzenski, A. B. Mahon, P. S. Arora, Nat. Protoc. 2010, 5, 1857.
- 41T. Vojkovsky, Pept. Res. 1995, 8, 236.
- 42D. Buckley, H. B. Henbest, P. Slade, J. Chem. Soc. 1957, 4891.
- 43R. E. Smith, W. R. Davis, Anal. Chem. 1984, 56, 2345.
- 44B. C. Smith, Spectroscopy 2019, 34, 22.
- 45S. Kim, A. M. Peterson, N. Holten-Andersen, Chem. Mater. 2018, 30, 3648.
- 46K. A. Curtis, D. Miller, P. Millard, S. Basu, F. Horkay, P. L. Chandran, PLoS One 2016, 11, e0158147.
- 47X. Yu, Z. Qin, H. Wu, H. Lv, X. Yang, Macromolecules 2019, 52, 1249.
- 48V. Yesilyurt, A. M. Ayoob, E. A. Appel, J. T. Borenstein, R. Langer, D. G. Anderson, Adv. Mater. 2017, 29, 1605947.
- 49D. A. Ossipov, S. Piskounova, O. P. Varghese, J. n. Hilborn, Biomacromolecules 2010, 11, 2247.
- 50S. Wang, O. P. Oommen, H. Yan, O. P. Varghese, Biomacromolecules 2013, 14, 2427.
- 51S. Hong, H. Lee, H. Lee, Beilstein J. Nanotechnol. 2014, 5, 887.
- 52G. C. Li, S. Y. Ma, M. Szostak, Trends Chem. 2020, 2, 914.
- 53W.-Z. Qiu, G.-P. Wu, Z.-K. Xu, ACS Appl. Mater. Interfaces 2018, 10, 5902.
- 54J. Yang, M. A. C. Stuart, M. Kamperman, Chem. Soc. Rev. 2014, 43, 8271.
- 55D. G. Barrett, D. E. Fullenkamp, L. He, N. Holten-Andersen, K. Y. C. Lee, P. B. Messersmith, Adv. Funct. Mater. 2013, 23, 1111.
- 56M. Bisaglia, S. Mammi, L. Bubacco, J. Biol. Chem. 2007, 282, 15597.
- 57B. P. Lee, J. L. Dalsin, P. B. Messersmith, Biomacromolecules 2002, 3, 1038.
- 58R. Mirshafian, W. Wei, J. N. Israelachvili, J. H. Waite, Biochemistry 2016, 55, 743.
- 59L. A. Burzio, J. H. Waite, Protein Sci. 2001, 10, 735.
- 60K. Wakamatsu, K. Nakao, H. Tanaka, Y. Kitahori, Y. Tanaka, M. Ojika, S. Ito, Int. J. Mol. Sci. 2019, 20, 2575.
- 61W. W. Weeks, M. P. Campos, S. Moldoveanu, J. Agric. Food Chem. 1993, 41, 1321.
- 62M. Salomäki, L. Marttila, H. Kivelä, T. Ouvinen, J. Lukkari, J. Phys. Chem. B 2018, 122, 6314.
- 63N. Vân Anh, R. M. Williams, Photochem. Photobiol. Sci. 2012, 11, 957.
- 64K. Molčanov, B. Kojić-Prodić, IUCrJ 2019, 6, 156.
- 65S. Hong, Y. S. Na, S. Choi, I. T. Song, W. Y. Kim, H. Lee, Adv. Funct. Mater. 2012, 22, 4711.
- 66S. Hong, Y. Wang, S. Y. Park, H. Lee, Sci. Adv. 2018, 4, eaat7457.
- 67S. H. Kim, J. W. Lee, I.-H. Yeo, Electrochim. Acta 2000, 45, 2889.
- 68J. H. Ryu, S. Hong, H. Lee, Acta Biomater. 2015, 27, 101.
- 69J. S. Lee, Y. S. Choi, J. S. Lee, E. J. Jeon, S. An, M. S. Lee, H. S. Yang, S.-W. Cho, Chem. Eng. J. 2022, 427, 130926.
- 70J. Shin, S. Choi, J. H. Kim, J. H. Cho, Y. Jin, S. Kim, S. Min, S. K. Kim, D. Choi, S. W. Cho, Adv. Funct. Mater. 2019, 29, 1903863.
- 71J. H. Maeng, B. W. Bang, E. Lee, J. Kim, H. G. Kim, D. H. Lee, S.-G. Yang, J. Mater. Sci.: Mater. Med. 2014, 25, 573.
- 72Y. Lee, T. E. Deelman, K. Chen, D. S. Lin, A. Tavakkoli, J. M. Karp, Nat. Mater. 2018, 17, 834.
- 73Y. Liang, M. Li, Y. Yang, L. Qiao, H. Xu, B. Guo, ACS Nano 2022, 16, 3194.
- 74X. Zhao, Y. Liang, Y. Huang, J. He, Y. Han, B. Guo, Adv. Funct. Mater. 2020, 30, 1910748.
- 75Y. Liang, Z. Li, Y. Huang, R. Yu, B. Guo, ACS Nano 2021, 15, 7078.
- 76M. Litwiniuk, A. Krejner, M. S. Speyrer, A. R. Gauto, T. Grzela, Wounds 2016, 28, 78.
- 77K. L. Aya, R. Stern, Wound Repair Regener. 2014, 22, 579.
- 78W. Ho, B. Tawil, J. C. Dunn, B. M. Wu, Tissue Eng. 2006, 12, 1587.
- 79J. P. Luyendyk, J. G. Schoenecker, M. J. Flick, Blood 2019, 133, 511.
- 80Y. Liu, K. Ai, L. Lu, Chem. Rev. 2014, 114, 5057.
- 81M. Guvendiren, P. B. Messersmith, K. R. Shull, Biomacromolecules 2008, 9, 122.
- 82S. An, E. J. Jeon, J. Jeon, S.-W. Cho, Mater. Horiz. 2019, 6, 1169.
- 83M.-C. Ku, C.-M. Fang, J.-T. Cheng, H.-C. Liang, T.-F. Wang, C.-H. Wu, C.-C. Chen, J.-H. Tai, S.-H. Chen, Sci. Rep. 2016, 6, 28804.
- 84Z. Xu, Sci. Rep. 2013, 3, 2914.
- 85Y. Wang, M. Xu, H. Dong, Y. Liu, P. Zhao, W. Niu, D. Xu, X. Ji, C. Xing, D. Lu, Acta Histochem. 2012, 114, 311.
- 86Y. Deng, J. Ren, G. Chen, G. Li, X. Wu, G. Wang, G. Gu, J. Li, Sci. Rep. 2017, 7, 2699.
- 87Q. Hou, W. Liu, Z. Liu, B. Duan, L. Bai, Carbohydr. Polym. 2008, 74, 235.
- 88X. Xia, K. F. Chan, G. T. Y. Wong, P. Wang, L. Liu, B. P. M. Yeung, E. K. W. Ng, J. Y. W. Lau, P. W. Y. Chiu, Sci. Transl. Med. 2019, 11, eaat7455.
- 89X. Xia, P. W. Y. Chiu, P. K. Lam, W. C. Chin, E. K. W. Ng, J. Y. W. Lau, Biochim. Biophys. Acta, Mol. Basis Dis. 2018, 1864, 178.
- 90H. Yuk, C. E. Varela, C. S. Nabzdyk, X. Mao, R. F. Padera, E. T. Roche, X. Zhao, Nature 2019, 575, 169.
- 91Y. Wang, E. J. Jeon, J. Lee, H. Hwang, S. W. Cho, H. Lee, Adv. Mater. 2020, 32, 2002118.
- 92K. Kim, H. Lee, S. Hong, J. Vis. Exp. 2016, e53930.