Effect of charge on in vivo adhesion stability of catechol-conjugated polysaccharides

Sang Hyeon Hong; Ji Hyun Ryu; Haeshin Lee

Journal of Industrial and Engineering Chemistry, Vol.79, 425-430, November, 2019

DOI10.1016/j.jiec.2019.07.017 Export Citation

Effect of charge on in vivo adhesion stability of catechol-conjugated polysaccharides

Sang Hyeon Hong, Ji Hyun Ryu^{1, †}, and Haeshin Lee^†

Department of Chemistry, Korea Advanced Institute of Science and Technology, Daejeon 34141, Republic of Korea
¹Department of Carbon Convergence Engineering, Wonkwang University, Iksan, Jeonbuk 54538, South Korea

E-mail:,

Mussel-inspired adhesive materials have received much attention for biomedical applications primarily because of their underwater/tissue adhesive properties. However, so far, no comparative study focusing on effect of charge differences (i.e., positive vs. negative) in the presence of conjugated catechols has been conducted. In this study, we investigate the physicochemical characteristics and in vitro/in vivo tissue adhesive properties of hydrogels that use anionic (i.e., hyaluronic acid) and cationic (i.e. chitosan) catechol-conjugated polysaccharides. Fe(III) is utilized to effectively prepare both hydrogels. Hyaluronic acid-catechol (HA-C) hydrogels are immediately formed by iron-catechol coordination bonds, while chitosan-catechol (CHI-C) hydrogel is formed by both iron-catechol coordination and catechol-amine covalent reactions. The gelation time and in vitro adhesiveness are similar for both CHI-C and HA-C hydrogels. Differences are found in that the CHI-C hydrogels showed enhanced water-resistance and long-lasting adhesion in vivo. It is noteworthy to mention that the cationic nature of mussel adhesive proteins due to lysine and histidine residues in the pads of Mytilus edulis is known to be an important contributor to underwater adhesion. Thus, this comparative study provides significant insight for the design of effective mussel-inspired adhesive materials.

Keywords:Hydrogel;Stability;Catechol;Chitosan;Hyaluronic acid

[References]

Lee BP, Messersmith PB, Israelachvili JN, Waite JH, Annu. Rev. Mater. Res., 41, 99 (2011)
Sedo J, Saiz-Poseu J, Busque F, Ruiz-Molina D, Adv. Mater., 25(5), 653 (2013)
Brubaker CE, Messersmith PB, Biomacromolecules, 12(12), 4326 (2011)
Lee BP, Dalsin JL, Messersmith PB, Biomacromolecules, 3(5), 1038 (2002)
Lee C, Shin J, Lee JS, Byun E, Ryu JH, Um SH, Kim DI, Lee H, Cho SW, Biomacromolecules, 14(6), 2004 (2013)
Kim JY, Ryu SB, Park KD, J. Ind. Eng. Chem., 58, 105 (2018)
Phuong PTM, Won HJ, Oh YJ, Lee HS, Lee KD, Park SY, J. Ind. Eng. Chem., (2019).
Lee H, Dellatore SM, Miller WM, Messersmith PB, Science, 318, 426 (2007)
Waite JH, J. Exp. Biol., 220, 517 (2017)
Hong SH, Wang Y, Park SY, Lee H, Sci. Adv., 4, eaat74 (2018)
Choe GH, Cho YH, Bae SM, Yoon SH, Lee JH, J. Ind. Eng. Chem., 73, 58 (2019)
Chen T, Yang M, Yang H, Wang R, Wang S, Zhang H, Zhang X, Zhao Z, Wang J, J. Ind. Eng. Chem., 69, 179 (2019)
Farzad E, Veisi H, J. Ind. Eng. Chem., 60, 114 (2018)
Kim E, Song IT, Lee S, Kim JS, Lee H, Jang JH, Angew. Chem.-Int. Edit., 51, 5598 (2012)
Jeong JH, Woo YJ, Lee MH, Haque MR, Ahn CH, Lee HS, Byun YR, J. Ind. Eng. Chem., 57, 330 (2018)
Clifford A, Lee BEJ, Grandfield K, Zhitomirsky I, Colloids Surf. B: Biointerfaces, 176, 115 (2019)
Krogsgaard M, Hansen MR, Birkedal H, J. Mater. Chem. B, 2, 8292 (2014)
Hong SH, Shin M, Lee J, Ryu JH, Lee S, Yang JW, Kim WD, Lee H, Adv. Healthcare Mater., 5, 75 (2016)
Lee J, Chang K, Kim S, Gite V, Chung H, Sohn, Macromolecules, 49, 750 (2016)
Min Y, Hammond PT, Chem. Mater., 23, 5349 (2011)
Yang Y, Qi P, Wen F, Li X, Xia Q, Maitz MF, Yang Z, Shen R, Tu Q, Huang N, ACS Appl. Mater. Interfaces, 6, 14608 (2014)
Joo H, Byun E, Lee M, Hong Y, Lee H, Kim P, J. Ind. Eng. Chem., 34, 14 (2016)
Birajdar MS, Halake KS, Lee JH, J. Ind. Eng. Chem., 63, 117 (2018)
Harrington MJ, Masic A, Holten-Andersen N, Waite JH, Fratzl P, Science, 328(5975), 216 (2010)
Lu Q, Hwang DS, Liu Y, Zeng H, Biomaterials, 33, 1903 (2012)
Salovaara S, Sandberg AS, Andlid T, J. Agric. Food Chem., 51, 7820 (2003)
Isayeva I, Das SS, Chang A, Defoe J, Luu HMD, Vorvolakos K, Patwardhan D, Whang J, Pollack S, J. Biomed. Mater. Res. B Appl. Biomater., 95, 9 (2010)
Andersena NH, Harrington MJ, Birkedal H, Lee BP, Messersmith PB, Lee KYC, Waite JH, Proceed. Natl. Acad. Sci. U. S. A., 108, 2651 (2011)
Fussell KC, Udasin RG, Smith PJS, Gallo MA, Laskin JD, Carcinogenesis, 32, 1285 (2011)
Schweigert N, Zehnder AJB, Eggen RIL, Environmental Microbiol., 3, 81 (2001)
Kalyanaraman B, Premovic PI, Sealy RC, J. Biol. Chem., 262, 11080 (1981)
Alegria AE, Sanchez-cruz P, Kumar A, Garcia C, Gonzalez FA, Orellano A, Zayas B, Gordaliza M, Free Radic. Res., 42, 70 (2008)
Faldt P, Bergenstahl B, Claesson PM, Colloids Surf. A: Physicochem. Eng. Asp., 71, 187 (1993)
Hurler J, Engesland A, Kermany BP, Skalko-Basnet N, J. Appl. Polym. Sci., 125(1), 180 (2012)
Prestwich GD, J. Control. Release, 155, 193 (2011)

[1] Lee BP, Messersmith PB, Israelachvili JN, Waite JH, Annu. Rev. Mater. Res., 41, 99 (2011)

[2] Sedo J, Saiz-Poseu J, Busque F, Ruiz-Molina D, Adv. Mater., 25(5), 653 (2013)

[3] Brubaker CE, Messersmith PB, Biomacromolecules, 12(12), 4326 (2011)

[4] Lee BP, Dalsin JL, Messersmith PB, Biomacromolecules, 3(5), 1038 (2002)

[5] Lee C, Shin J, Lee JS, Byun E, Ryu JH, Um SH, Kim DI, Lee H, Cho SW, Biomacromolecules, 14(6), 2004 (2013)

[6] Kim JY, Ryu SB, Park KD, J. Ind. Eng. Chem., 58, 105 (2018)

[7] Phuong PTM, Won HJ, Oh YJ, Lee HS, Lee KD, Park SY, J. Ind. Eng. Chem., (2019).

[8] Lee H, Dellatore SM, Miller WM, Messersmith PB, Science, 318, 426 (2007)

[9] Waite JH, J. Exp. Biol., 220, 517 (2017)

[10] Hong SH, Wang Y, Park SY, Lee H, Sci. Adv., 4, eaat74 (2018)

[11] Choe GH, Cho YH, Bae SM, Yoon SH, Lee JH, J. Ind. Eng. Chem., 73, 58 (2019)

[12] Chen T, Yang M, Yang H, Wang R, Wang S, Zhang H, Zhang X, Zhao Z, Wang J, J. Ind. Eng. Chem., 69, 179 (2019)

[13] Farzad E, Veisi H, J. Ind. Eng. Chem., 60, 114 (2018)

[14] Kim E, Song IT, Lee S, Kim JS, Lee H, Jang JH, Angew. Chem.-Int. Edit., 51, 5598 (2012)

[15] Jeong JH, Woo YJ, Lee MH, Haque MR, Ahn CH, Lee HS, Byun YR, J. Ind. Eng. Chem., 57, 330 (2018)

[16] Clifford A, Lee BEJ, Grandfield K, Zhitomirsky I, Colloids Surf. B: Biointerfaces, 176, 115 (2019)

[17] Krogsgaard M, Hansen MR, Birkedal H, J. Mater. Chem. B, 2, 8292 (2014)

[18] Hong SH, Shin M, Lee J, Ryu JH, Lee S, Yang JW, Kim WD, Lee H, Adv. Healthcare Mater., 5, 75 (2016)

[19] Lee J, Chang K, Kim S, Gite V, Chung H, Sohn, Macromolecules, 49, 750 (2016)

[20] Min Y, Hammond PT, Chem. Mater., 23, 5349 (2011)

[21] Yang Y, Qi P, Wen F, Li X, Xia Q, Maitz MF, Yang Z, Shen R, Tu Q, Huang N, ACS Appl. Mater. Interfaces, 6, 14608 (2014)

[22] Joo H, Byun E, Lee M, Hong Y, Lee H, Kim P, J. Ind. Eng. Chem., 34, 14 (2016)

[23] Birajdar MS, Halake KS, Lee JH, J. Ind. Eng. Chem., 63, 117 (2018)

[24] Harrington MJ, Masic A, Holten-Andersen N, Waite JH, Fratzl P, Science, 328(5975), 216 (2010)

[25] Lu Q, Hwang DS, Liu Y, Zeng H, Biomaterials, 33, 1903 (2012)

[26] Salovaara S, Sandberg AS, Andlid T, J. Agric. Food Chem., 51, 7820 (2003)

[27] Isayeva I, Das SS, Chang A, Defoe J, Luu HMD, Vorvolakos K, Patwardhan D, Whang J, Pollack S, J. Biomed. Mater. Res. B Appl. Biomater., 95, 9 (2010)

[28] Andersena NH, Harrington MJ, Birkedal H, Lee BP, Messersmith PB, Lee KYC, Waite JH, Proceed. Natl. Acad. Sci. U. S. A., 108, 2651 (2011)

[29] Fussell KC, Udasin RG, Smith PJS, Gallo MA, Laskin JD, Carcinogenesis, 32, 1285 (2011)

[30] Schweigert N, Zehnder AJB, Eggen RIL, Environmental Microbiol., 3, 81 (2001)

[31] Kalyanaraman B, Premovic PI, Sealy RC, J. Biol. Chem., 262, 11080 (1981)

[32] Alegria AE, Sanchez-cruz P, Kumar A, Garcia C, Gonzalez FA, Orellano A, Zayas B, Gordaliza M, Free Radic. Res., 42, 70 (2008)

[33] Faldt P, Bergenstahl B, Claesson PM, Colloids Surf. A: Physicochem. Eng. Asp., 71, 187 (1993)

[34] Hurler J, Engesland A, Kermany BP, Skalko-Basnet N, J. Appl. Polym. Sci., 125(1), 180 (2012)

[35] Prestwich GD, J. Control. Release, 155, 193 (2011)