Restoration of articular osteochondral defects in rat by a bi-layered hyaluronic acid hydrogel plug with TUDCA-PLGA microsphere

Byoung Ju Kim; Yoshie Arai; Bogyu Choi; Sunghyun Park; Jinsung Ahn; In-Bo Han; Soo-Hong Lee

Journal of Industrial and Engineering Chemistry, Vol.61, 295-303, May, 2018

DOI10.1016/j.jiec.2017.12.027 Export Citation

Restoration of articular osteochondral defects in rat by a bi-layered hyaluronic acid hydrogel plug with TUDCA-PLGA microsphere

Byoung Ju Kim, Yoshie Arai, Bogyu Choi, Sunghyun Park, Jinsung Ahn, In-Bo Han^{1, †}, and Soo-Hong Lee^†

Department of Biomedical Science, CHA University, CHA Biocomplex, 335, Pangyo-ro, Bundang-gu, Seongnam-si, Gyeonggi-do, 13488, Republic of Korea
¹Department of Neurosurgery,, CHA University, CHA Bundang Medical Center, 59, Yatap-ro, Bundang-gu, Seongnam-si, Gyeonggi-do, 13496, Republic of Korea

E-mail:,

Tauroursodeoxycholic acid (TUDCA) has a role in the regulation of the differentiation of mesenchymal stem cells. In this study, TUDCA was demonstrated to increase osteogenic differentiation at a low concentration (25 μM) and chondrogenic differentiation at a high concentration (2500 μM). We investigated the regeneration of osteochondral defects in a rat model using a bilayer plug loaded with two different concentration of TUDCA-PLGA microspheres (TUDCA-MS bilayer plug). The TUDCA-MS bilayer plug successfully regenerated cartilage and subchondral bone layer. Therefore, we suggest that the TUDCA-MS bilayer plug as a new treatment method for simultaneous regeneration of cartilage and subchondral bone layer.

Keywords:Tauroursodeoxycholic acid;Stem cell differentiation;Microsphere;Bi-layered hydrogel;Osteoarthritis

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Lu HH, Subramony SD, Boushell MK, Zhang X, Ann. Biomed. Eng., 38, 2142 (2010)
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Sottile V, Seuwen K, Febs Lett., 475, 201 (2000)
Liu LF, Shen WJ, Zhang ZH, Wang LJ, Kraemer FB, J. Cell Physiol., 225, 837 (2010)
Cha BH, Jung MJ, Moon BK, Kim JS, Ma Y, Arai Y, Noh M, Shin JY, Kim BS, Lee SH, Bone, 83, 73 (2016)
Benz C, Angermuller S, Tox U, Kloters-Plachky P, Riedel HD, Sauer P, Stremmel W, Stiehl A, J. Hepatol., 28, 99 (1998)
Benz C, Angermuller S, Otto G, Sauer P, Stremmel W, Stiehl A, Eur. J. Clin. Invest., 30, 203 (2000)
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Park JH, Kwon DY, Heo JY, Park SH, Park JY, Lee B, Kim JH, Kim MS, Tissue Eng. Regen. Med., 14, 743 (2017)
Mahapatra C, Jin GZ, Kim HW, Tissue Eng. Regen. Med., 13, 538 (2016)
Makadia HK, Siegel SJ, Polymer, 3, 1377 (2011)
Kang SW, Bada LP, Kang CS, Lee JS, Kim CH, Park JH, Kim BS, Biotechnol. Lett., 30(3), 435 (2008)
Kim B, Kim DW, Kim S, Cho J, Lee H, Park D, Park S, Choi B, Min BH, Osteoarthritis Cartilage, 21 (2013)
Shim YB, Jung HH, Jang JW, Yang HS, Bae H, Park JC, Choi B, Lee SH, J. Ind. Eng. Chem., 37, 101 (2016)
Kim BJ, Choi BH, Jin LH, Park SR, Min BH, Tissue Eng. Regen. Med., 10, 211 (2013)
Khademhosseini A, Vacanti JP, Langer R, Sci. Am., 300, 64 (2009)
Goldring MB, Ther. Adv. Musculoskelet. Dis., 4, 269 (2012)
Lajeunesse D, Osteoarthritis Cartilage, 12, S34 (2004)
Xavier JM, Morgado AL, Rodrigues CM, Sola S, ABBV Cell Cycle, 13, 3576 (2014)
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Albalak A, Zeidel ML, Zucker SD, Jackson AA, Donovan JM, Biochemistry, 35, 7936 (1996)
Li YM, Schilling T, Benisch P, Zeck S, Meissner-Weigl J, Schneider D, Limbert C, Seufert J, Kassem M, Schutze N, Jakob F, Ebert R, Biochem. Biophys. Res. Commun., 363(1), 209 (2007)
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[Referenced By]

[1] Li G, Yin J, Gao J, Cheng TS, Pavlos NJ, Zhang C, Zheng MH, Arthritis Res. Ther., 15, 223 (2013)

[2] Hunziker EB, Osteoarthritis Cartilage, 10, 432 (2002)

[3] Tampieri A, Sprio S, Sandri M, Valentini F, Trends Biotechnol., 29, 526 (2011)

[4] Lynn AK, Best SM, Cameron RE, Harley BA, Yannas IV, Gibson LJ, Bonfield W, J. Biomed. Mater. Res. A, 92, 1057 (2010)

[5] Jiang J, Tang A, Ateshian GA, Guo XE, Hung CT, Lu HH, Ann. Biomed. Eng., 38, 2183 (2010)

[6] Grayson WL, Chao PHG, Marolt D, Kaplan DL, Vunjak-Novakovic G, Trends Biotechnol., 26, 181 (2008)

[7] Mano J, Reis R, J. Tissue Eng. Regen. Med., 1, 261 (2007)

[8] Oliveira JM, Rodrigues MT, Silva SS, Malafaya PB, Gomes ME, Viegas CA, Dias IR, Azevedo JT, Mano JF, Reis RL, Biomaterials, 27, 6123 (2006)

[9] Nakajima H, Goto T, Horikawa O, Kikuchi T, Shinmei M, Histochem. Cell Biol., 109, 331 (1998)

[10] Buckwalter JA, Brown TD, Clin. Orthop. Rel. Res., 423, 7 (2004)

[11] Lu HH, Subramony SD, Boushell MK, Zhang X, Ann. Biomed. Eng., 38, 2142 (2010)

[12] Chen J, Chen H, Li P, Diao H, Zhu S, Dong L, Wang R, Guo T, Zhao J, Zhang J, Biomaterials, 32, 4793 (2011)

[13] Giannoni P, Lazzarini E, Ceseracciu L, Barone AC, Quarto R, Scaglione S, J. Tissue Eng. Regen. Med., 9, 1182 (2015)

[14] James AW, LaChaud G, Shen J, Asatrian G, Nguyen V, Zhang X, Ting K, Soo C, Tissue Eng. Part B Rev., 22, 284 (2016)

[15] Raida M, Clement JH, Leek RD, Ameri K, Bicknell R, Niederwieser D, Harris AL, J. Cancer Res. Clin. Oncol., 131, 741 (2005)

[16] Reyes R, Pec MK, Sanchez E, del Rosario C, Delgado A, Evora C, Eur. Cell Mater., 25, 351 (2013)

[17] Rivard AL, Steer CJ, Kren BT, Rodrigues CM, Castro RE, Bianco RW, Low WC, Am. J. Chin. Med., 35, 279 (2007)

[18] Yanguas-Casas N, Barreda-Manso MA, Nieto-Sampedro M, Romero-Ramirez L, J. Neuroinflammation, 11, 50 (2014)

[19] Heubi JE, Wiechmann DA, Creutzinger V, Setchell KD, Squires R, Couser R, Rhodes P, J. Pediatr., 141, 237 (2002)

[20] Steiner C, Othman A, Saely CH, Rein P, Drexel H, von Eckardstein A, Rentsch KM, PLoS One, 6, e25006 (2011)

[21] Keene CD, Rodrigues CM, Eich T, Chhabra MS, Steer CJ, Low WC, Proc. Natl. Acad. Sci. U. S. A., 99, 10671 (2002)

[22] Drack AV, Dumitrescu AV, Bhattarai S, Gratie D, Stone EM, Mullins R, Sheffield VC, Invest. Ophthalmol. Vis. Sci., 53, 100 (2012)

[23] Castro RE, Sola S, Ramalho RM, Steer CJ, Rodrigues CM, J. Pharmacol. Exp. Ther., 311, 845 (2004)

[24] Schoemaker MH, de la Rosa LC, Buist-Homan M, Vrenken TE, Havinga R, Poelstra K, Haisma HJ, Jansen PJ, Moshage H, Hepatology, 39, 1563 (2004)

[25] Ramalho RM, Viana RJ, Low WC, Steer CJ, Rodrigues CM, Trends Mol. Med., 14, 54 (2008)

[26] Cha BH, Kim JS, Ahn JC, Kim HC, Kim BS, Han DK, Park SG, Lee SH, Biomaterials, 35, 2851 (2014)

[27] Cho JG, Lee JH, Hong SH, Lee HN, Kim CM, Kim SY, Yoon KJ, Oh BJ, Kim JH, Jung SY, Asahara T, Kwon SM, Park SG, Stem Cells, 33, 792 (2015)

[28] Savopoulos C, Dokos C, Kaiafa G, Hatzitolios A, Hippokratia, 15, 18 (2011)

[29] Sottile V, Seuwen K, Febs Lett., 475, 201 (2000)

[30] Liu LF, Shen WJ, Zhang ZH, Wang LJ, Kraemer FB, J. Cell Physiol., 225, 837 (2010)

[31] Cha BH, Jung MJ, Moon BK, Kim JS, Ma Y, Arai Y, Noh M, Shin JY, Kim BS, Lee SH, Bone, 83, 73 (2016)

[32] Benz C, Angermuller S, Tox U, Kloters-Plachky P, Riedel HD, Sauer P, Stremmel W, Stiehl A, J. Hepatol., 28, 99 (1998)

[33] Benz C, Angermuller S, Otto G, Sauer P, Stremmel W, Stiehl A, Eur. J. Clin. Invest., 30, 203 (2000)

[34] Xie Q, Khaoustov VI, Chung CC, Sohn J, Krishnan B, Lewis DE, Yoffe B, Hepatology, 36, 592 (2002)

[35] Ulery BD, Nair LS, Laurencin CT, J. Polym. Sci. B: Polym. Phys., 49(12), 832 (2011)

[36] Park JH, Kwon DY, Heo JY, Park SH, Park JY, Lee B, Kim JH, Kim MS, Tissue Eng. Regen. Med., 14, 743 (2017)

[37] Mahapatra C, Jin GZ, Kim HW, Tissue Eng. Regen. Med., 13, 538 (2016)

[38] Makadia HK, Siegel SJ, Polymer, 3, 1377 (2011)

[39] Kang SW, Bada LP, Kang CS, Lee JS, Kim CH, Park JH, Kim BS, Biotechnol. Lett., 30(3), 435 (2008)

[40] Kim B, Kim DW, Kim S, Cho J, Lee H, Park D, Park S, Choi B, Min BH, Osteoarthritis Cartilage, 21 (2013)

[41] Shim YB, Jung HH, Jang JW, Yang HS, Bae H, Park JC, Choi B, Lee SH, J. Ind. Eng. Chem., 37, 101 (2016)

[42] Kim BJ, Choi BH, Jin LH, Park SR, Min BH, Tissue Eng. Regen. Med., 10, 211 (2013)

[43] Khademhosseini A, Vacanti JP, Langer R, Sci. Am., 300, 64 (2009)

[44] Goldring MB, Ther. Adv. Musculoskelet. Dis., 4, 269 (2012)

[45] Lajeunesse D, Osteoarthritis Cartilage, 12, S34 (2004)

[46] Xavier JM, Morgado AL, Rodrigues CM, Sola S, ABBV Cell Cycle, 13, 3576 (2014)

[47] Soares R, Ribeiro FF, Xapelli S, Genebra T, Ribeiro MF, Sebastiao AM, Rodrigues CMP, Sola S, Mol. Neurobiol. (2017).

[48] Panella C, Ierardi E, De Marco MF, Barone M, Guglielmi FW, Polimeno L, Francavilla A, Ital. J. Gastroenterol., 27, 256 (1995)

[49] Alpini G, Baiocchi L, Glaser S, Ueno Y, Marzioni M, Francis H, Phinizy JL, Angelico M, Lesage G, Hepatology, 35, 1041 (2002)

[50] Albalak A, Zeidel ML, Zucker SD, Jackson AA, Donovan JM, Biochemistry, 35, 7936 (1996)

[51] Li YM, Schilling T, Benisch P, Zeck S, Meissner-Weigl J, Schneider D, Limbert C, Seufert J, Kassem M, Schutze N, Jakob F, Ebert R, Biochem. Biophys. Res. Commun., 363(1), 209 (2007)

[52] Zolnik BS, Burgess DJ, J. Control. Release, 122, 338 (2007)