3D printed cell-laden collagen and hybrid scaffolds for in vivo articular cartilage tissue regeneration

YoungWon Koo; Eun-Ji Choi; JaeYoon Lee; Han-Jun Kim; GeunHyung Kim; Sun Hee Do

Journal of Industrial and Engineering Chemistry, Vol.66, 343-355, October, 2018

DOI10.1016/j.jiec.2018.05.049 Export Citation

3D printed cell-laden collagen and hybrid scaffolds for in vivo articular cartilage tissue regeneration

YoungWon Koo, Eun-Ji Choi¹, JaeYoon Lee, Han-Jun Kim¹, GeunHyung Kim^†, and Sun Hee Do^{1, †}

College of Biotechnology and Bioengineering, Sungkyunkwan University, Suwon, Gyeonggi, Republic of Korea
¹College of Veterinary Medicine, Konkuk University, Seoul, Republic of Korea

E-mail:,

Current surgical treatments for osteochondral injuries include chondrocyte transplantation, osteochondral grafts, and bone marrow stimulation. Despite these approaches, repaired tissues often show limited regeneration resulting in fibrocartilage formation with poor mechanical properties. To overcome these shortcomings, a regenerative cell-laden scaffold therapy is a promising treatment option. In this study, we propose a three-dimensional (3D) micro-sized mesh structure using a cell-laden collagen bioink. To achieve the optimal cell-printing condition for the fabrication of cell-laden collagen structure, porous mesh collagen scaffold (PMCS) were assessed for the mechanical properties, printability and cell viability analysis. In vivo regenerative effects of PMCS were compared to the injecting hydrogel without pores (non-porous collagen scaffold (NPCS)), collagen/poly(e-caprolactone) (PCL) hybrid scaffold (CPHS)), and pure PCL scaffold (PPS). The porous mesh-structured/cell-laden collagen scaffold (PMCS) showed significantly enhanced cartilage regeneration in vivo compared to other conditions.

Keywords:Collagen;Cell-laden scaffold;Cell-printing;Hybrid scaffold;Osteochondral regeneration

[References]

Makris EA, Gomoll AH, Malizos KN, Hu JC, Athanasiou KA, Nat. Rev. Rheumatol., 11, 21 (2015)
Fennema E, Rivron N, Rouwkema J, van Blitterswijk C, de Boer J, Trends Biotechnol., 31, 108 (2013)
Knight E, Przyborski S, J. Anat., 227, 746 (2015)
Ouyang L, Yao R, Zhao Y, Sun W, Biofabrication, 8, 035020 (2016)
Murphy SV, Atala A, Nat. Biotechnol., 32, 773 (2014)
Li Y, Cheng H, Cheung K, Chan D, Chan B, Acta Biomater., 10, 1919 (2014)
Mullen LM, Best SM, Ghose S, Wardale J, Rushton N, Cameron RE, J. Mater. Sci., 26, 2 (2015)
Enea D, Cecconi S, Calcagno S, Busilacchi A, Manzotti S, Gigante A, Knee, 22, 30 (2015)
Kim YB, Lee H, Kim GH, ACS Appl. Mater. Interfaces, 8, 32230 (2016)
Gelman R, Williams BR, Piez K, J. Biol. Chem., 254, 180 (1979)
Pederson AW, Ruberti JW, Messersmith PB, Biomaterials, 24, 4881 (2003)
Yoon H, Lee JS, Yim H, Kim G, Chun W, RSC Adv., 6, 21439 (2016)
Liang HC, Chang WH, Lin KJ, Sung HW, J. Biomed. Mater. Res. A, 65, 271 (2003)
Moffat KL, Marra KG, J. Biomed. Mater. Res. B Appl. Biomater., 71, 181 (2004)
Rothrauff BB, Coluccino L, Gottardi R, Ceseracciu L, Scaglione S, Goldoni L, Tuan RS, J. Tissue Eng. Regen. Med. (2017).
Revell CM, Athanasiou KA, Tissue Eng. B Rev., 15, 1 (2008)
Meng F, Zhang Z, Huang G, Chen W, Zhang Z, He A, Liao W, Eur. Cell Mater., 31, 79 (2016)
Kuroda R, Ishida K, Matsumoto T, Akisue T, Fujioka H, Mizuno K, Ohgushi H, Wakitani S, Kurosaka M, Osteoarthritis Cartilage, 15, 226 (2007)
Zhang L, Yuan T, Guo L, Zhang X, J. Biomed. Mater. Res. A, 100, 2717 (2012)
Yang J, Zhang YS, Yue K, Khademhosseini A, Acta Biomater., 57, 1 (2017)
Oliveira JT, Santos TC, Martins L, Picciochi R, Marques AP, Castro AG, Neves NM, Mano JF, Reis RL, Tissue Eng. A, 16, 343 (2009)
Kim YB, Lee H, Yang GH, Choi CH, Lee D, Hwang H, Jung WK, Yoon H, Kim GH, J. Colloid Interface Sci., 461, 359 (2016)
Lee H, Han W, Kim H, Ha DH, Jang J, Kim BS, Cho DW, Biomacromolecules, 18(4), 1229 (2017)
Seol YJ, Park JY, Jeong W, Kim TH, Kim SY, Cho DW, J. Biomed. Mater. Res. A, 103, 1404 (2015)
Mintz BR, Cooper JA, J. Biomed. Mater. Res. A, 102, 2918 (2014)
Yeo M, Kim G, J. Mater. Chem. B, 2, 6830 (2014)
Yoshimura K, Chonan Y, Shirai K, Nihon Chikusan Gakkaiho, 70, 227 (1999)
Lai G, Li Y, Li G, Int. J. Biol. Macromol., 42, 285 (2008)
Shannon G, Novak T, Mousoulis C, Voytik-Harbin S, Neu C, RSC Adv., 5, 2113 (2015)
Hospodiuk M, Dey M, Sosnoski D, Ozbolat IT, Biotechnol. Adv., 35, 217 (2017)
Panwar A, Tan LP, Molecules, 21, 685 (2016)
Kong HJ, Smith MK, Mooney DJ, Biomaterials, 24, 4023 (2003)
Yu Y, Zhang Y, Martin JA, Ozbolat IT, J. Biomech. Eng., 135, 901011 (2013)
Hutmacher DW, Scaffolds in Tissue Engineering Bone and Cartilage, Elsevier, pp.175 2006.
Leong K, Cheah C, Chua C, Biomaterials, 24, 2363 (2003)
Tarafder S, Balla VK, Davies NM, Bandyopadhyay A, Bose S, J. Tissue Eng. Regener. Med., 7, 631 (2013)
Ke D, Dernell W, Bandyopadhyay A, Bose S, J. Biomed. Mater. Res. B Appl. Biomater., 103, 1549 (2015)
Nehrer S, Breinan H, Ramappa A, Hsu H, Minas T, Shortkroff S, Sledge C, Yannas I, Spector M, Biomaterials, 19, 2313 (1998)
Grigolo B, Roseti L, Fiorini M, Fini M, Giavaresi G, Aldini NN, Giardino R, Facchini A, Biomaterials, 22, 2417 (2001)
Lee CH, Cook JL, Mendelson A, Moioli EK, Yao H, Mao JJ, Lancet, 376, 440 (2010)
Cancedda R, Dozin B, Giannoni P, Quarto R, Matrix Biol., 22, 81 (2003)
Pirlo RK, Wu P, Liu J, Ringeisen B, Biotechnol. Bioeng., 109(1), 262 (2012)

[Referenced By]

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

[2] Fennema E, Rivron N, Rouwkema J, van Blitterswijk C, de Boer J, Trends Biotechnol., 31, 108 (2013)

[3] Knight E, Przyborski S, J. Anat., 227, 746 (2015)

[4] Ouyang L, Yao R, Zhao Y, Sun W, Biofabrication, 8, 035020 (2016)

[5] Murphy SV, Atala A, Nat. Biotechnol., 32, 773 (2014)

[6] Li Y, Cheng H, Cheung K, Chan D, Chan B, Acta Biomater., 10, 1919 (2014)

[7] Mullen LM, Best SM, Ghose S, Wardale J, Rushton N, Cameron RE, J. Mater. Sci., 26, 2 (2015)

[8] Enea D, Cecconi S, Calcagno S, Busilacchi A, Manzotti S, Gigante A, Knee, 22, 30 (2015)

[9] Kim YB, Lee H, Kim GH, ACS Appl. Mater. Interfaces, 8, 32230 (2016)

[10] Gelman R, Williams BR, Piez K, J. Biol. Chem., 254, 180 (1979)

[11] Pederson AW, Ruberti JW, Messersmith PB, Biomaterials, 24, 4881 (2003)

[12] Yoon H, Lee JS, Yim H, Kim G, Chun W, RSC Adv., 6, 21439 (2016)

[13] Liang HC, Chang WH, Lin KJ, Sung HW, J. Biomed. Mater. Res. A, 65, 271 (2003)

[14] Moffat KL, Marra KG, J. Biomed. Mater. Res. B Appl. Biomater., 71, 181 (2004)

[15] Rothrauff BB, Coluccino L, Gottardi R, Ceseracciu L, Scaglione S, Goldoni L, Tuan RS, J. Tissue Eng. Regen. Med. (2017).

[16] Revell CM, Athanasiou KA, Tissue Eng. B Rev., 15, 1 (2008)

[17] Meng F, Zhang Z, Huang G, Chen W, Zhang Z, He A, Liao W, Eur. Cell Mater., 31, 79 (2016)

[18] Kuroda R, Ishida K, Matsumoto T, Akisue T, Fujioka H, Mizuno K, Ohgushi H, Wakitani S, Kurosaka M, Osteoarthritis Cartilage, 15, 226 (2007)

[19] Zhang L, Yuan T, Guo L, Zhang X, J. Biomed. Mater. Res. A, 100, 2717 (2012)

[20] Yang J, Zhang YS, Yue K, Khademhosseini A, Acta Biomater., 57, 1 (2017)

[21] Oliveira JT, Santos TC, Martins L, Picciochi R, Marques AP, Castro AG, Neves NM, Mano JF, Reis RL, Tissue Eng. A, 16, 343 (2009)

[22] Kim YB, Lee H, Yang GH, Choi CH, Lee D, Hwang H, Jung WK, Yoon H, Kim GH, J. Colloid Interface Sci., 461, 359 (2016)

[23] Lee H, Han W, Kim H, Ha DH, Jang J, Kim BS, Cho DW, Biomacromolecules, 18(4), 1229 (2017)

[24] Seol YJ, Park JY, Jeong W, Kim TH, Kim SY, Cho DW, J. Biomed. Mater. Res. A, 103, 1404 (2015)

[25] Mintz BR, Cooper JA, J. Biomed. Mater. Res. A, 102, 2918 (2014)

[26] Yeo M, Kim G, J. Mater. Chem. B, 2, 6830 (2014)

[27] Yoshimura K, Chonan Y, Shirai K, Nihon Chikusan Gakkaiho, 70, 227 (1999)

[28] Lai G, Li Y, Li G, Int. J. Biol. Macromol., 42, 285 (2008)

[29] Shannon G, Novak T, Mousoulis C, Voytik-Harbin S, Neu C, RSC Adv., 5, 2113 (2015)

[30] Hospodiuk M, Dey M, Sosnoski D, Ozbolat IT, Biotechnol. Adv., 35, 217 (2017)

[31] Panwar A, Tan LP, Molecules, 21, 685 (2016)

[32] Kong HJ, Smith MK, Mooney DJ, Biomaterials, 24, 4023 (2003)

[33] Yu Y, Zhang Y, Martin JA, Ozbolat IT, J. Biomech. Eng., 135, 901011 (2013)

[34] Hutmacher DW, Scaffolds in Tissue Engineering Bone and Cartilage, Elsevier, pp.175 2006.

[35] Leong K, Cheah C, Chua C, Biomaterials, 24, 2363 (2003)

[36] Tarafder S, Balla VK, Davies NM, Bandyopadhyay A, Bose S, J. Tissue Eng. Regener. Med., 7, 631 (2013)

[37] Ke D, Dernell W, Bandyopadhyay A, Bose S, J. Biomed. Mater. Res. B Appl. Biomater., 103, 1549 (2015)

[38] Nehrer S, Breinan H, Ramappa A, Hsu H, Minas T, Shortkroff S, Sledge C, Yannas I, Spector M, Biomaterials, 19, 2313 (1998)

[39] Grigolo B, Roseti L, Fiorini M, Fini M, Giavaresi G, Aldini NN, Giardino R, Facchini A, Biomaterials, 22, 2417 (2001)

[40] Lee CH, Cook JL, Mendelson A, Moioli EK, Yao H, Mao JJ, Lancet, 376, 440 (2010)

[41] Cancedda R, Dozin B, Giannoni P, Quarto R, Matrix Biol., 22, 81 (2003)

[42] Pirlo RK, Wu P, Liu J, Ringeisen B, Biotechnol. Bioeng., 109(1), 262 (2012)