Injectable thermoresponsive hydrogel/nanofiber hybrid scaffolds inducing human adipose-derived stem cell chemotaxis

Youngjoo Choi; Min Hee Park; Kangwon Lee

Journal of Industrial and Engineering Chemistry, Vol.82, 89-97, February, 2020

DOI10.1016/j.jiec.2019.09.046 Export Citation

Injectable thermoresponsive hydrogel/nanofiber hybrid scaffolds inducing human adipose-derived stem cell chemotaxis

Youngjoo Choi, Min Hee Park^{1, †}, and Kangwon Lee^†

Department of Transdisciplinary Studies, Graduate School of Convergence Science and Technology, Seoul National University, Seoul 08826, Republic of Korea
¹Center for Convergence Bioceramic Materials, Korea Institute of Ceramic Engineering and Technology, Cheongju 28160, Republic of Korea

E-mail:,

Hydrogels with three-dimensional networks similar to extracellular matrix (ECM) have been widely investigated as biomaterials in tissue engineering. Injectable hydrogels have been studied for less invasive treatments, and moreover, the endogenous cell recruitment capability can create synergy with these hydrogels for repairing damaged tissues. However, their low mechanical properties or difficult process has been a disadvantage for their use in load-bearing cartilage such as intervertebral disc. Therefore, high-modulus injectable hydrogels which have the potential in cell recruitment are required for fundamental and less invasive treatments. In this study, we fabricated injectable and thermoresponsive hybrid scaffolds comprising chitosan/gelatin hydrogel and polycaprolactone nanofibers, and we added platelet-derived growth factor-BB (PDGF-BB) within the hybrid scaffolds to recruit human adipose-derived stem cells (hADSCs). The modulus of the hybrid scaffolds was approximately 0.9 MPa after gelation at 37 °C with structural similarity to the ECM. Also the modulus could be managed by changing the concentration of the components in the hybrid scaffolds. The release of PDGF-BB from the hybrid scaffolds induced hADSC chemotaxis under rough condition which chemoattractant was diluted by serum free cell culture medium. Our proposed hybrid scaffolds are promising candidates for less invasive tissue engineering strategies to induce endogenous hADSC recruitment.

Keywords:Injectable hydrogel;Thermoresponsive hydrogel;Cell recruitment;Adipose-derived stem cells;Biomaterials;Drug releasing

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[1] Liu M, Zeng X, Ma C, Yi H, Ali Z, Mou XB, Li S, Deng Y, He NY, Bone Res., 5 (2017)

[2] Hoffman AS, Adv. Drug Deliv. Rev., 64, 18 (2012)

[3] Vedadghavami A, Minooei F, Mohammadi MH, Khetani S, Kolahchi AR, Mashayekhan S, Sanati-Nezhad A, Acta Biomater., 62, 42 (2017)

[4] Dashtimoghadam E, Mirzadeh H, Taromi FA, Nystrom B, RSC Adv., 4, 39386 (2014)

[5] Ji CD, Shi J, Mater. Sci. Eng. C-Biomimetic Supramol. Syst., 33, 3780 (2013)

[6] Chetouani A, Follain N, Marais S, Rihouey C, Elkolli M, Bounekhel M, Benachour D, Le Cerf D, Int. J. Biol. Macromol., 97, 348 (2017)

[7] Sasson A, Patchornik S, Eliasy R, Robinson D, Haj-Ali R, J. Mech. Behav. Biomed., 8, 143 (2012)

[8] Saraiva SM, Miguel SP, Ribeiro MP, Coutinho P, Correia IJ, RSC Adv., 5, 63478 (2015)

[9] Cheng NC, Lin WJ, Ling TY, Young TH, Acta Biomater., 51, 258 (2017)

[10] Wang CS, Virgilio N, Wood-Adams PM, Heuzey MC, Food Hydrocoll., 79, 462 (2018)

[11] Wise JK, Yarin AL, Megaridis CM, Cho M, Tissue Eng. A, 15, 913 (2009)

[12] Xue RY, Qian YN, Li LH, Yao GD, Yang L, Sun YP, Stem Cell Res. Ther., 8 (2017)

[13] Borjigin M, Strouse B, Niamat RA, Bialk P, Eskridge C, Xie JW, Kmiec EB, Mol. Ther. Nucl. Acids, 1 (2012)

[14] Sharma C, Dinda AK, Potdar PD, Chou CF, Mishra NC, Mater. Sci. Eng. C-Biomimetic Supramol. Syst., 64, 416 (2016)

[15] Hamedi H, Moradi S, Hudson SM, Tonelli AE, Carbohydr. Polym., 199, 445 (2018)

[16] Ko IK, Lee SJ, Atala A, Yoo JJ, Exp. Mol. Med., 45 (2013)

[17] Yu Y, Wu RX, Yin Y, Chen FM, J. Mater. Chem. B, 4, 569 (2016)

[18] Makris EA, Gomoll AH, Malizos KN, Hu JC, Athanasiou KA, Nat. Rev. Rheumatol., 11, 21 (2015)

[19] Grayson WL, Bunnell BA, Martin E, Frazier T, Hung BP, Gimble JM, Nat. Rev. Endocrinol., 11, 140 (2015)

[20] Tsuruma K, Yamauchi M, Sugitani S, Otsuka T, Ohno Y, Nagahara Y, Ikegame Y, Shimazawa M, Yoshimura S, Iwama T, Hara H, Stem Cell Transl. Med., 3, 42 (2014)

[21] Tsuji W, Rubin JP, Marra KG, World J. Stem Cells, 6, 312 (2014)

[22] Fontana G, Thomas D, Collin E, Pandit A, Adv. Healthc. Mater., 3, 2012 (2014)

[23] Fani N, Farokhi M, Azami M, Kamali A, Bakhshaiesh NL, Ebrahimi-Barough S, Ai J, Eslaminejad MB, ACS Biomater. Sci. Eng., 5, 2134 (2019)

[24] Liu ZQ, Wang HB, Wang Y, Lin QX, Yao AN, Cao F, Li DX, Zhou J, Duan CM, Du ZY, Wang YM, Wang CY, Biomaterials, 33, 3093 (2012)

[25] Lai FY, Kakudo N, Morimoto N, Taketani S, Hara T, Ogawa T, Kusumoto K, Stem Cell Res. Ther., 9 (2018)

[26] Zhao Y, Zhang H, Cytotherapy, 18, 816 (2016)

[27] Xie ZW, Paras CB, Weng H, Punnakitikashem P, Su LC, Vu K, Tang LP, Yang J, Nguyen KT, Acta Biomater., 9, 9351 (2013)

[28] Salha S, Gehmert S, Brebant V, Anker A, Loibl M, Prantl L, Gehmert S, Clin. Hemorheol. Microcirc., 70, 543 (2018)

[29] Wagner B, Gorin Y, Am. J. Physiol. Renal., 306, F85 (2014)

[30] Kim S, Shin BH, Yang C, Jeong S, Shim JH, Park MH, Choy YB, Heo CY, Lee K, Polym. Basel, 10 (2018)

[31] Phipps MC, Xu YY, Bellis SL, PLoS One, 7 (2012)

[32] Yoon D, Kim H, Lee E, Park MH, Chung S, Jeon H, Ahn CH, Lee K, Biomater. Res., 20, 25 (2016)

[33] Ryu YJ, Cho TJ, Lee DS, Choi JY, Cho J, Mol. Cells, 35, 557 (2013)

[34] Ge JF, Guo L, Wang S, Zhang YL, Cai T, Zhao RCH, Wu YJ, Stem Cell Rev. Rep., 10, 295 (2014)

[35] Wang JH, Yang Q, Cheng NM, Tao XJ, Zhang ZH, Sun XM, Zhang QQ, Mater. Sci. Eng. C-Biomimetic Supramol. Syst., 61, 705 (2016)

[36] Chen WM, Ma J, Zhu L, Morsi Y, EI-Hamshary H, Al-Deyab SS, Mo XM, Colloids Surf. B: Biointerfaces, 142, 165 (2016)

[37] Mouw JK, Ou GQ, Weaver VM, Nat. Rev. Mol. Cell Biol., 15, 771 (2014)

[38] Zhang XH, Reagan MR, Kaplan DL, Adv. Drug Deliv. Rev., 61, 988 (2009)

[39] Nguyen LTB, Odeleye AOO, Chui CY, Baudequin T, Cui ZF, Ye H, Sci. Rep., 9 (2019)

[40] Araujo JV, Martins A, Leonor IB, Pinho ED, Reis RL, Neves NM, J. Biomater. Sci.-Polym. Ed., 19, 1261 (2008)

[41] Kalaf EAG, Pendyala M, Bledsoe JG, Sell SA, J. Mech. Behav. Biomed. Mater., 72, 229 (2017)

[42] Recuerda M, Perie D, Gilbert G, Beaudoin G, BMC Musculoskelet Disord., 13, 195 (2012)

[43] Armentano I, Dottori M, Fortunati E, Mattioli S, Kenny JM, Polym. Degrad. Stabil., 95, 2126 (2010)

[44] Sun HF, Mei L, Song CX, Cui XM, Wang PY, Biomaterials, 27, 1735 (2006)