Highly effective induction of cell-derived extracellular matrix by macromolecular crowding for osteogenic differentiation of mesenchymal stem cells

Yong-In Yoo; Kyoung-Won Ko; Seung-Gyu Cha; So-Yeon Park; Jiwon Woo; Dong Keun Han

Journal of Industrial and Engineering Chemistry, Vol.107, 391-400, March, 2022

DOI10.1016/j.jiec.2021.12.008 Export Citation

Highly effective induction of cell-derived extracellular matrix by macromolecular crowding for osteogenic differentiation of mesenchymal stem cells

Yong-In Yoo¹, Kyoung-Won Ko¹, Seung-Gyu Cha¹, So-Yeon Park^{1, 2}, Jiwon Woo¹, and Dong Keun Han^{1, †}

¹Department of Biomedical Science, CHA University, 335 Pangyo-ro, Bundang-gu, Seongnam, Gyeonggi 13488, Republic of Korea
²Division of Biotechnology, Korea University, 145 Anam-ro, Seongbuk-gu, Seoul 02841, Republic of Korea

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The extracellular matrix (ECM) is the non-cellular component that exists in all tissues and provides dynamic microenvironment that initiates crucial biochemical and biophysical cues, including cell adhesion, proliferation, migration, and differentiation. Although the cell-derived ECM mimics the native cellular microenvironment, the long-term maintenance of cells is required to harvest a sufficient amount of ECM for the intended application. In this study, we evaluated the biophysical properties of fucoidan as a macromolecular crowding (MMC) agent to accelerate ECM synthesis and deposition in human dermal fibroblasts and found that the accumulated cell-derived ECM by fucoidan (fCDM) influenced the osteogenic differentiation of mesenchymal stem cells (MSCs). The treatment of fucoidan resulted in significantly higher ECM deposition at 5 days compared with the treatment of dextran sulfate (DxS), a potent MMC agent. The advantages of fCDM were demonstrated in vitro by the promotion of multiple cellular behaviors of MSCs, osteogenic differentiation, and signal transduction pathway. In addition, the PLGA scaffold containing fCDM had significantly higher alkaline phosphatase activity than the PLGA scaffold containing acellular bone tissue ECM. Based on these results, the fCDM can support the development of human cell-derived, xeno-free biomaterials for tissue engineering applications.

Keywords:Macromolecular crowding;Fucoidan;Human cell-derived ECM;Mesenchymal stem cells;Osteogenic differentiation

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[2] Blair HC, Larrouture QC, Li Y, Lin H, Beer-Stoltz D, Liu L, Tuan RS, Robinson LJ, Schlesinger PH, Nelson DJ, Tissue Eng. Part B Rev., 23, 268 (2017)

[3] Pirraco RP, Cerqueira MT, Reis RL, Marques AP, Cytotherapy, 14, 1276 (2012)

[4] Kim IG, Hwang MP, Du P, Ko J, Ha CW, Do SH, Park K, Biomaterials, 50, 75 (2015)

[5] Larsen M, Artym VV, Green JA, Yamada KM, Curr. Opin. Cell Biol., 18, 463 (2006)

[6] Chun SY, Lim JO, Lee EH, Han MH, Ha YS, Lee JN, Kim BS, Park MJ, Yeo M, Jung B, Kwon TG, Tissue Eng. Regen. Med., 16, 385 (2019)

[7] Tran HD, Park KD, Ching YC, Huynh C, Nguyen DH, J. Ind. Eng. Chem., 89, 58 (2020)

[8] Liao J, Guo X, Grande-Allen KJ, Kasper FK, Mikos AG, Biomaterials, 31, 8911 (2010)

[9] Maia FR, Reis RL, Oliveira JM, Methods Cell Biol., 156, 45 (2020)

[10] Harris GM, Raitman I, Schwarzbauer JE, Methods Cell Biol., 143, 97 (2018)

[11] Bourget JM, Gauvin R, Larouche D, Lavoie A, Labbe R, Auger FA, Germain L, Biomaterials, 33, 9205 (2012)

[12] Hoshiba T, J. Mater. Chem. B, 5, 4322 (2017)

[13] Ahlfors JE, Billiar KL, Biomaterials, 28, 2183 (2007)

[14] Falanga V, Zhou L, Yufit T, J. Cell. Physiol., 191, 42 (2002)

[15] Bateman JF, Pillow JJ, Mascara T, Medvedec S, Ramshaw JA, Cole WG, Biochem. J., 245, 677 (1987)

[16] Zeiger AS, Loe FC, Li R, Raghunath M, Van Vliet KJ, PLoS ONE, 7, e37904 (2012)

[17] Satyam A, Tsokos MG, Tresback JS, Zeugolis DI, Tsokos GC, Adv. Funct. Mater., 30, 1908752 (2020)

[18] Kuznetsova IM, Turoverov KK, Uversky VN, Int. J. Mol. Sci., 15, 23090 (2014)

[19] Graham J, Raghunath M, Vogel V, Biomater. Sci., 7, 4519 (2019)

[20] Chen C, Loe F, Blocki A, Peng Y, Raghunath M, Adv. Drug Deliv. Rev., 63, 277 (2011)

[21] Gaspar D, Fuller KP, Zeugolis DI, Acta Biomater., 88, 197 (2019)

[22] Cavanzo NP, Bigaeva E, Boersema M, Olinga P, Bank RA, Front. Med. (Lausanne), 7, 615774 (2020)

[23] Shendi D, Marzi J, Linthicum W, Rickards AJ, Dolivo DM, Keller S, Kauss MA, Wen Q, McDevitt TC, Dominko T, Schenke-Layland K, Rolle MW, Acta Biomater., 100, 292 (2019)

[24] Gaspar D, Ryan CNM, Zeugolis DI, Faseb J., 33, 5741 (2019)

[25] De Pieri A, Rana S, Korntner S, Zeugolis DI, Int. J. Biol. Macromol., 164, 434 (2020)

[26] Graceffa V, Zeugolis DJEC, Eur. Cells Mater., 37, 310 (2019)

[27] Takada T, Katagiri T, Ifuku M, Morimura N, Kobayashi M, Hasegawa K, Ogamo A, Kamijo R, J. Biol. Chem., 278, 43229 (2003)

[28] Dong R, Bai Y, Dai J, Deng M, Zhao C, Tian Z, Zeng F, Liang W, Liu L, Dong S, Tissue Eng., 11, 1 (2020)

[29] Lee DJ, Miguez P, Kwon J, Daniel R, Padilla R, Min S, Zalal R, Ko CC, Shin HW, Tissue Eng., 11 (2020)

[30] Zheng C, Chen J, Liu S, Jin Y, Int. J. Oral Sci., 11, 23 (2019)

[31] Zhu M, Li W, Dong X, Yuan X, Midgley AC, Chang H, Wang Y, Wang H, Wang K, Ma PX, Wang H, Kong D, Nat. Commun., 10, 4620 (2019)

[32] Tantra R, Schulze P, Quincey P, Particuology, 8, 279 (2010)

[33] Lareu RR, Subramhanya KH, Peng Y, Benny P, Chen C, Wang Z, Rajagopalan R, Raghunath M, Febs Lett., 581, 2709 (2007)

[34] Yao Q, Zheng YW, Lan QH, Kou L, Xu HL, Zhao YZ, Mater. Sci. Eng. C-Biomimetic Supramol. Syst., 104, 109942 (2019)

[35] Popov C, Radic T, Haasters F, Prall WC, Aszodi A, Gullberg D, Schieker M, Docheva D, Cell Death Dis., 2, e186 (2011)

[36] Becerra-Bayona SM, Guiza-Arguello VR, Russell B, Hook M, Hahn MS, J. Biomed. Mater. Res. A, 106, 2594 (2018)

[37] Liu Y, Wang H, Dou H, Tian B, Li L, Jin L, Zhang Z, Hu L, Tissue Eng., 11, 1 (2020)

[38] Lee E, Ko JY, Kim J, Park JW, Lee S, Im GI, Biomater. Sci., 7, 4588 (2019)

[39] Tang T, Feinberg T, Keller ET, Li XY, Weiss SJ, Nat. Cell Biol., 18, 917 (2016)

[40] Lorthongpanich C, Thumanu K, Tangkiettrakul K, Jiamvoraphong N, Laowtammathron C, Damkham N, Issaragrisil UPYS, Stem Cell Res. Ther, 10, 402 (2019)

[41] Yang L, Gao Q, Ge L, Zhou Q, Warszawik EM, Bron R, Lai KWC, van Rijn R, Biomater. Sci., 8, 2638 (2020)