Micro-groove patterned PCL patches with DOPA for rat Achilles tendon regeneration

Sihyeon Park; Min Suk Lee; Jin Jeon; Juhan Lim; Chris Hyunchul Jo; Suk Ho Bhang; Hee Seok Yang

Journal of Industrial and Engineering Chemistry, Vol.105, 352-364, January, 2022

DOI10.1016/j.jiec.2021.09.037 Export Citation

Micro-groove patterned PCL patches with DOPA for rat Achilles tendon regeneration

Sihyeon Park¹, Min Suk Lee¹, Jin Jeon¹, Juhan Lim¹, Chris Hyunchul Jo², Suk Ho Bhang³, and Hee Seok Yang^{1, 4, †}

¹Department of Nanobiomedical Science & BK21 FOUR NBM Global Research Center for Regenerative Medicine, Dankook University, Cheonan 31116, Republic of Korea
²Department of Orthopedic Surgery, SMG-SNU Boramae Medical Center, Seoul National University College of Medicine, 20 Boramae-ro 5-gil, Dongjak-gu, Seoul 07061, Republic of Korea
³School of Chemical Engineering, Sungkyunkwan University, Suwon 16419, Republic of Korea
⁴Center for Bio-Medical Engineering Core-Facility, Dankook University, Cheonan 31116, Republic of Korea

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Achilles tendon regeneration using current tissue engineering techniques requires morphometrically mimetic tendon biomaterials to attain the required microstructural tendon tissue and to achieve the necessary mechanical properties. In this study, we used nano- (400 nm) and micro-groove (5000 nm) patterned polycaprolactone patches (PCL-400, PCL-5000), which offer adequate elastic modulus and biocompatibility. The PCL patches were fabricated via capillary force lithography and were surface modified with 3,4-dihydroxy-L-phenylalanine (DOPA) for increased hydrophilicity. We hypothesized that the resulting biologically surface-modified elastic groove patterned patches would enhance the cell behaviors in vitro and the rat Achilles tendon regeneration in vivo. The micro-groove patterned PCL patches with DOPA coating (DOPA-PCL-5000) exhibited excellent cell elongation, tenogenic differentiation and YAP expression of the mesenchymal stem cells in our in vitro study and these results were further confirmed by application to the rat Achilles tendon rupture model in our in vivo study. DOPA-PCL-5000 induced dramatic regeneration of rat Achilles tendon compared to the other groups, which was further confirmed by the Achilles functional index and histological analysis at 8 weeks. In conclusion, DOPAPCL-5000 can be used not only for damaged Achilles tendon, but also for various functional tendon regeneration techniques such as rotator cuff, patellar tendon, and flexor tendon.

Keywords:Polycaprolactone;Groove pattern;Topographical cue;3,4-Dihydroxy-L-phenylalanine;Tenogenic differentiation;Achilles tendon

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[1] Beldjilali-Labro M, Garcia AG, Farhat F, Bedoui F, Grosset JF, Dufresne M, Legallais C, Materials, 11 (2018)

[2] Sheng D, Li J, Ai C, Feng S, Ying T, Liu X, Cai J, Ding X, Jin W, Xu H, Chen J, Chen S, J. Mater. Chem. B, 7, 4801 (2019)

[3] Puetzer JL, Ma T, Sallent I, Gelmi A, Stevens MM, Biomaterials (2020).

[4] Lin J, Zhou W, Han S, Bunpetch V, Zhao K, Liu C, Yin Z, Ouyang H, Acta Biomater., 70, 1 (2018)

[5] Evrova O, Burgisser GM, Ebnother C, et al., Biomaterials, 232 (2020)

[6] Sebastin SJ, Ho A, Karjalainen T, Chung KC, J. Hand Surg. Am., 38, 552 (2013)

[7] Docheva D, Muller SA, Majewski M, Evans CH, Adv. Drug Deliv. Rev., 84, 222 (2015)

[8] Kim DH, Provenzano PP, Smith CL, Levchenko A, J. Cell Biol., 197, 351 (2012)

[9] Kim HN, Jiao A, HWang NS, Kim MS, Kang DH, Kim DH, Suh KY, Adv. Drug Deliv. Rev., 65, 536 (2013)

[10] Bettinger CJ, Langer R, Borenstein JT, Angew. Chem.-Int. Edit., 48, 5406 (2009)

[11] Kshitiz, Afzal J, Kim SY, Kim DH, Cell Adh. Migr., 9, 300 (2015)

[12] Haeger A, Wolf K, Zegers MM, Friedl P, Trends Cell Biol., 25, 556 (2015)

[13] Dasgupta I, McCollum D, J. Biol. Chem., 294, 17693 (2019)

[14] Elosegui-Artola A, Andreu I, Beedle AEM, et al., Cell, 171(1397-14) (2017)

[15] Tomas AR, Goncalves AI, Paz E, Freitas P, Domingues RMA, Gomes ME, Nanoscale, 11, 18255 (2019)

[16] Kim DH, Provenzano PP, Smith CL, Levchenko A, J. Cell Biol., 197, 351 (2012)

[17] Patel M, Hong HJ, Koh WG, J. Ind. Eng. Chem., 80, 729 (2019)

[18] Park SH, Choi KS, Kim DU, Kim WC, Lee DH, Kim HN, Hyun H, Lim KT, Kim JW, Kim YR, Kim JH, J. Ind. Eng. Chem., 61, 65 (2018)

[19] Forooshani PK, Lee BP, J. Polym. Sci. A: Polym. Chem., 55(1), 9 (2017)

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

[21] Bajetto A, Pattarozzi A, Corsaro A, Barbieri F, Daga A, Bosio A, Gatti M, Pisaturo V, Sirito R, Florio T, Front. Cell. Neurosci., 11, 312 (2017)

[22] Amiri F, Halabian R, Salimian M, Shokrgozar MA, Soleimani M, Jahanian-Najafabadi A, Roudkenar MH, Cell Stress Chaperones, 19, 657 (2014)

[23] Komatsu I, Wang JH, Iwasaki K, Shimizu T, Okano T, Acta Biomater., 42, 136 (2016)

[24] Murrell GA, Lilly EG, Davies H, Best TM, Goldner RD, Seaber AV, J. Orthop. Res., 10, 398 (1992)

[25] Voleti PB, Buckley MR, Soslowsky LJ, Annu. Rev. Biomed. Eng., 14, 47 (2012)

[26] Kandasamy K, Narayanan K, Ni M, Du C, Wan ACA, Zink D, Biomacromolecules, 15(6), 2067 (2014)

[27] Yang K, Lee JS, Kim J, Lee YB, Shin H, Um SH, Kim JB, Park KI, Lee H, Cho SW, Biomaterials, 33, 6952 (2012)

[28] Saiz-Poseu J, Mancebo-Aracil J, Nador F, Busque F, Ruiz-Molina D, Angew. Chem.-Int. Edit., 58, 696 (2019)

[29] Chen S, Bai B, Lee DJ, Diachina S, Li Y, Wong SW, Wang Z, Tseng HC, Ko CC, J. Stem Cell Res. Ther., 7 (2017)

[30] Xi ZY, Xu YY, Zhu LP, Wang Y, Zhu BK, J. Membr. Sci., 327(1-2), 244 (2009)

[31] Janorkar AV, Fritz EW, Burg KJ, Metters AT, Hirt DE, J. Biomed. Mater. Res. B Appl. Biomater., 81, 142 (2007)

[32] Sensini A, Cristofolini L, Materials, 11 (2018)

[33] Sobral JM, Malheiro VN, Clyne TW, Harris J, Rezk R, O’Neill W, Markaki AE, J. Mech. Behav. Biomed. Mater., 60, 22 (2016)

[34] Wang X, Faria-Briceno JJ, Busani T, Brueck SRJ, J. Vac. Sci. Technol. B, 37 (2019)

[35] Cheng CT, To S, Zhang G, J. Ind. Eng. Chem., 91, 69 (2020)

[36] Diaz JP, Valenzuela MA, Blanco IV, Lopez SJ, Cuesta MP, Garcia O, Jimenez ED, Casarrubios JS, Cristache C, Am. Soc. Mech. Eng., V07AT08A027 (2013).

[37] Leelamanie D, Karube J, Yoshida A, Soil Sci. Plant Nutr., 54, 695 (2008)

[38] Webb K, Hlady V, Tresco PA, J. Biomed. Mater. Res., 41, 422 (1998)

[39] Yang S, Shi X, Li X, Wang J, Wang Y, Luo Y, Biomaterials, 207, 61 (2019)

[40] Wang Z, Lee WJ, Koh BTH, Hong M, Wang W, Lim PN, Feng J, Park LS, Kim M, Thian ES, Sci. Adv., 4, eaat45 (2018)

[41] Lee MS, Lee DH, Jeon J, Oh SH, Yang HS, ACS Appl. Mater. Interfaces, 10, 38780 (2018)

[42] Yoon JK, Kim HN, Bhang SH, Shin JY, Han J, La WG, Jeong GJ, Kang S, Lee JR, Oh J, Kim MS, Jeon NL, Kim BS, Tissue Eng. Part A, 22, 6554 (2016)

[43] Mierke CT, AIMS Biophys., 4, 615 (2017)

[44] Yang K, Jung K, Ko E, Kim J, Park KI, Kim J, Cho SW, ACS Appl. Mater. Interfaces, 5, 10529 (2013)

[45] Kim J, Kim HN, Lim KT, Kim Y, Pandey S, Garg P, Choung YH, Choung PH, Suh KY, Chung JH, Biomaterials, 34, 7257 (2013)

[46] Du W, Du W, Wan M, Zhou X, Xu X, Zheng L, Curr. Stem Cell Res. Ther., 13, 16 (2018)

[47] Nardone G, Oliver-De La Cruz J, Vrbsky J, et al.,, Nat. Commun., 8, 15321 (2017)

[48] Li W, Midgley AC, Bai Y, Zhu M, Chang H, Zhu W, Wang L, Wang Y, Wang H, Kong D, Biomaterials, 224 (2019)

[49] Webb WR, Dale TP, Lomas AJ, Zeng G, Wimpenny I, El Haj AJ, Forsyth NR, Chen GQ, Biomaterials, 34, 6683 (2013)

[50] Park U, Lee MS, Jeon J, Lee S, Hwang MP, Wang Y, Yang HS, Kim K, Acta Biomater., 90, 179 (2019)