Three-dimensional printed biomimetic multilayer scaffolds coordinated with sleep-related small extracellular vesicles: A strategy for extracellular matrix homeostasis andmacrophage polarization to enhance osteochondral regeneration

Xu-Ran Li; Qing-Song Deng; Po-Lin Liu; Shu-Hang He; Yuan Gao; Zhan-Ying Wei; Chang-Ru Zhang; Fei Wang; Xiao-Qiu Dou; Helen Dawes; Shang-Chun Guo; Shi-Cong Tao

doi:10.1002/VIW.20230069

VIEW ›› 2024, Vol. 5 ›› Issue (2) : 20230069 DOI: 10.1002/VIW.20230069

RESEARCH ARTICLE

Three-dimensional printed biomimetic multilayer scaffolds coordinated with sleep-related small extracellular vesicles: A strategy for extracellular matrix homeostasis andmacrophage polarization to enhance osteochondral regeneration

Xu-Ran Li ¹^,²^,³
, Qing-Song Deng ¹^,²^,³
, Po-Lin Liu ¹^,²^,³
, Shu-Hang He ¹^,²^,³
, Yuan Gao ¹^,²^,³
, Zhan-Ying Wei ⁴
, Chang-Ru Zhang ⁵^,⁶
, Fei Wang ⁷
, Xiao-Qiu Dou ⁸
, Helen Dawes ⁹^,¹⁰^,¹¹
, Shang-Chun Guo ¹^,²^,³^,^†
, Shi-Cong Tao ¹^,²^,^†

Author information +

¹. Department of Orthopedic Surgery, Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai, China

². School of Medicine, Shanghai Jiao Tong University, Shanghai, China

³. Institute of Microsurgery on Extremities, Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai, China

⁴. Shanghai Clinical Research Centre of Bone Diseases, Department of Osteoporosis and Bone Diseases, Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai, China

⁵. Shanghai Key Laboratory of Orthopedic Implants, Department of Orthopedic Surgery, Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China

⁶. Clinical and Translational Research Center for 3D Printing Technology, Medical 3D Printing Innovation Research Center, Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China

⁷. Department of Orthopedics, Shanghai Key Laboratory for Prevention and Treatment of Bone and Joint Diseases, Shanghai Institute of Traumatology and Orthopedics, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China

⁸. State Key Lab of Metal Matrix Composites, School of Materials Science and Engineering, Shanghai Jiao Tong University, Shanghai, China

⁹. Faculty of Health and Life Science, Oxford Brookes University, Oxford, UK

¹⁰. NIHR Oxford Health Biomedical Research Centre, Oxford, UK

¹¹. College of Medicine and Health, St Lukes Campus, University of Exeter, Exeter, UK

scguo@shsmu.edu.cn

sctao@shsmu.edu.cn

Show less

History +

PDF

Abstract

Cartilage defects resulting from injury or degeneration are a common clinical problem, and due to its avascular nature, articular cartilage has poor self-healing capacity. Three-dimensional (3D) bioprinting has attracted great attention in tissue engineering. Melatonin (MT), a hormone mainly secreted at night, plays an important role in tissue repair. Small extracellular vesicles (sEV) are considered ideal drug delivery vehicles and MT-sEV (sleep-related sEV) have the potential ability to promote cartilage regeneration. Here, biomimetic multilayer scaffolds were fabricated using 3D bioprinting. A double network hydrogel, composed of methacrylated hyaluronic acid and gelatin methacryloyl (HG), was prepared. MT-sEV and HG hydrogel were used to create a cartilage layer. A bone layer was formed using poly(ϵ-caprolactone) and hydroxyapatite ultralong nanowires. Additionally, two bioinks were alternately printed at the interface layer. The results of RNA sequencing revealed the potential regulatory mechanisms. MTsEV showed promotional effects on cell migration, proliferation, chondrogenic differentiation, and extracellular matrix (ECM) deposition. Moreover, MT-sEV altered macrophage polarization and regulated the expression of inflammatory cytokines. In vivo experiments demonstrated that the biomimetic multilayer scaffolds promoted cartilage regeneration. These experiments demonstrated the ability of MT-sEV to regulate the immune microenvironment and promote the secretion of ECM, providing a promising strategy for cartilage regeneration.

Keywords

3D bioprinting / cartilage regeneration / cartilage tissue engineering / hydrogels / small extracellular vesicles

Cite this article

Download citation ▾

Xu-Ran Li, Qing-Song Deng, Po-Lin Liu, Shu-Hang He, Yuan Gao, Zhan-Ying Wei, Chang-Ru Zhang, Fei Wang, Xiao-Qiu Dou, Helen Dawes, Shang-Chun Guo, Shi-Cong Tao. Three-dimensional printed biomimetic multilayer scaffolds coordinated with sleep-related small extracellular vesicles: A strategy for extracellular matrix homeostasis andmacrophage polarization to enhance osteochondral regeneration. VIEW, 2024, 5(2): 20230069 DOI:10.1002/VIW.20230069

登录浏览全文

4963

注册一个新账户忘记密码

References

Publishing order | Descend order by publishing year | Descend order by cited within

[1]	B.Xu, J.Ye, F.-Z.Yuan, J.-Y. Zhang, Y.-R.Chen, B.-S.Fan, D.Jiang, W.-B.Jiang, X. Wang, J.-K.Yu, Front. Bioeng. Biotechnol. 2020, 8, 247.

[2]	C.Becher, M. A.Malahias, M. M.Ali, N.Maffulli, H.Thermann, Knee Surg. Sports Traumatol. Arthrosc. 2019, 27, 2731.

[3]	J.Elayyan, I.Carmon, L.Zecharyahu, G.Batshon, Y. H.Maatuf, E.Reich, M.Dumont, L.Kandel, M.Klutstein, M.Dvir-Ginzberg, Proc. Natl.Acad. Sci. U. S. A. 2022, 119, e2116855119.

[4]	M.-L.Ji, H.Jiang, Z.Li, R.Geng, J. Z.Hu, Y. C. Lin, J.Lu, Nat. Commun. 2022, 13, 7658.

[5]	Y.Lei, X.Wang, J.Liao, J. Shen, Y.Li, Z.Cai, N.Hu, X.Luo, W. Cui, W.Huang, Bioactive Mater. 2022, 16, 472.

[6]	T. L.Fernandes, A. H.Gomoll, C.Lattermann, A. J.Hernandez, D. F.Bueno, M. T.Amano, Front. Immunol. 2020, 11, 111.

[7]	J.Yin, H.Zeng, K.Fan, H. Xie, Y.Shao, Y.Lu, J.Zhu, Z.Yao, L. Liu, H.Zhang, B.Luo, X.Wang, C.Zeng, X. Bai, H.Zhang, D.Cai, Cell Death. Dis. 2022, 13, 567.

[8]	J.Yang, X.Zhang, J.Chen, B. C. Heng, Y.Jiang, X.Hu, Z.Ge, J. Cell. Physiol. 2022, 237, 2258.

[9]	S.Wang, S.Zhao, J.Yu, Z.Gu, Y.Zhang, Small 2022, 18, e2201869.

[10]	J.Wang, D.Huang, H.Yu, Y.Cheng, H.Ren, Y. Zhao, Eng. Regen. 2022, 3, 80.

[11]	Y.Zhu, B.Kong, R.Liu, Y. Zhao, Smart Med. 2022, 1, e20220006.

[12]	C.Li, W.Zhang, Y.Nie, D. Jiang, J.Jia, W.Zhang, L.Li, Z.Yao, L. Qin, Y.Lai, Adv. Funct. Mater. 2023, 33, 2214158.

[13]	Y.Liu, L.Peng, L.Li, C.Huang, K.Shi, X. Meng, P.Wang, M.Wu, L.Li, H.Cao, K. Wu, Q.Zeng, H.Pan, W. W.Lu, L.Qin, C. Ruan, X.Wang, Biomaterials 2021, 279, 121216.

[14]	C.Meng, D.Tang, X.Liu, J. Meng, W.Wei, R. H.Gong, J.Li, Int. J. Biol. Macromol. 2023, 235, 123781.

[15]	G.-J.Huang, H.-P.Yu, X.-L.Wang, B.-B. Ning, J.Gao, Y.-Q.Shi, Y.-J.Zhu, J.-L.Duan, J. Mater. Chem. B 2021, 9, 1277.

[16]	H.Hong, Y. B.Seo, D. Y.Kim, J. S. Lee, Y. J.Lee, H.Lee, O.Ajiteru, M. T.Sultan, O. J.Lee, S. H.Kim, C. H.Park, Biomaterials 2020, 232, 119679.

[17]	M.Wang, J.Zhao, Y.Luo, Q. Liang, Y.Liu, G.Zhong, Y.Yu, F.Chen, Macromol. Biosci. 2022, 22, 2200179.

[18]	B.Velasco-Rodriguez, T. Diaz-Vidal, L. CRosales-Rivera, C. A.García-González, C.Alvarez-Lorenzo, A. Al-Modlej, V.Dominguez-Arca, G.Prieto, S.Barbosa, J. F. A.Soltero Martínez, P.Taboada, Int. J. Mol. Sci. 2021, 22, 6758.

[19]	D. C. SCosta, P. D. C. Costa, M. C.Gomes, A.Chandrakar, P. A.Wieringa, L.Moroni, J. F.Mano, ACS Mater. Lett. 2022, 4, 701.

[20]	Y.Wu, X.Zhang, B.Tan, Y. Shan, X.Zhao, J.Liao, Biomater. Adv. 2022, 133, 112641.

[21]	M. S.Kang, M.Kwon, S. H.Lee, W.-H. Kim, G. W.Lee, H. J.Jo, B.Kim, S. Y.Yang, K. S. Kim, D.-W.Han, Chem. Asian J. 2022, 17, e202200620.

[22]	L. K.Shopperly, J.Spinnen, J.-P.Kruger, M.Endres, M.Sittinger, T.Lam, L.Kloke, T.Dehne, J. Biomed. Mater. Res., Part B 2022, 110, 2310.

[23]	Y.Wang, F.Wen, X.Yao, L. Zeng, J.Wu, Q.He, H.Li, L.Fang, Front. Bioeng. Biotechnol. 2021, 9, 811652.

[24]	S.Pahoff, C.Meinert, O.Bas, L.Nguyen, T. J.Klein, D. W.Hutmacher, J. Mater. Chem. B 2019, 7, 1761.

[25]	N.Nowak, T.Gaisl, D.Miladinovic, R.Marcinkevics, M.Osswald, S.Bauer, J.Buhmann, R.Zenobi, P.Sinues, S. A.Brown, M.Kohler, Cell Rep. 2021, 37, 109903.

[26]	D.Zada, Y.Sela, N.Matosevich, A.Monsonego, T.Lerer-Goldshtein, Y.Nir, L.Appelbaum, Mol. Cell 2021, 81, 4979.

[27]	M.Chennaoui, T.Vanneau, A.Trignol, P.Arnal, D.Gomez-Merino, C.Baudot, J.Perez, S.Pochettino, C.Eirale, H.Chalabi, J. Sci. Med. Sport 2021, 24, 982.

[28]	J.Liu, Q.Sun, M.Sun, L. Lin, X.Ren, T.Li, Q.Xu, Z.Sun, J. Duan, Free Rad. Biol. Med. 2022, 181, 166.

[29]	K.-H.Lu, P. W.-A. Lu, E. W.-H.Lu, C.-H.Tang, S.-C.Su, C.-W.Lin, S.-F. Yang, J. Pineal Res. 2021, 71, e12762.

[30]	S.-C.Tao, J.-Y.Huang, Y.Gao, Z.-X. Li, Z.-Y.Wei, H.Dawes, S.-C.Guo, Bioactive Mater. 2021, 6, 4455.

[31]	E. C.Beck, M.Barragan, M. H.Tadros, S. H.Gehrke, M. S.Detamore, Acta Biomater. 2016, 38, 94.

[32]	F.Malekipour, D.Oetomo, P. V.-S.Lee, J. Biomech. 2016, 49, 2053.

[33]	Y.Wang, J.Wang, R.Gao, X. Liu, Z.Feng, C.Zhang, P.Huang, A.Dong, D. Kong, W.Wang, Biomaterials 2022, 285, 121538.

[34]	X.Zhou, Y.Qian, L.Chen, T. Li, X.Sun, X.Ma, J.Wang, C.He, ACS Nano 2023, 17, 5140.

[35]	Q.Zhang, X.Zhou, H.Du, Y.Ha, Y.Xu, R.Ao, C.He, ACS Biomater. Sci. Eng. 2023, 9, 4583.

[36]	S.-C.Tao, T.Yuan, Y.-L.Zhang, W.-J. Yin, S.-C.Guo, C.-Q.Zhang, Theranostics 2017, 7, 180.

[37]	P. P.Marie, S.-J.Fan, J.Mason, A. Wells, C. C.Mendes, S. M.Wainwright, S. Scott, R.Fischer, A. L.Harris, C.Wilson, D. C. I.Goberdhan, J. Extracell. Vesicles 2023, 12, e12311.

[38]	P.Chen, L.Zheng, Y.Wang, M. Tao, Z.Xie, C.Xia, C.Gu, J.Chen, P. Qiu, S.Mei, L.Ning, Y.Shi, C.Fang, S. Fan, X.Lin, Theranostics 2019, 9, 2439.

[39]	S.Kim, J.-C.Lee, E.-S.Cho, J. Kwon, J. Cell. Biochem. 2013, 114, 2513.

[40]	S.Koelling, J.Kruegel, M.Irmer, J. R.Path, B.Sadowski, X.Miro, N.Miosge, Cell Stem Cell 2009, 4, 324.

[41]	K.Choocheep, S.Hatano, H.Takagi, H.Watanabe, K.Kimata, P.Kongtawelert, H.Watanabe, J. Biol. Chem. 2010, 285, 21114.

[42]	J.Zhu, S.Yang, Y.Qi, Z.Gong, H.Zhang, K. Liang, P.Shen, Y.-Y.Huang, Z.Zhang, W.Ye, L.Yue, S.Fan, S. Shen, A. G.Mikos, X.Wang, X.Fang, Sci. Adv. 2022, 8, eabk0011.

[43]	D.Vallejo, F.Hernández-Torres, E.Lozano-Velasco, L.Rodriguez-Outeiriño, A.Carvajal, C.Creus, D.Franco, A. E. Aránega, Stem Cell Rep. 2018, 10, 1398.

[44]	S.Bai, Y.Wei, W.Hou, Y. Yao, J.Zhu, X.Hu, W.Chen, Y.Du, W.He, B.Shen, J. Du, BMJ Open Diabetes Res. Care 2020, 8, e001400.

[45]	F.Motta, E.Barone, A.Sica, C.Selmi, Clin. Rev.Allergy Immunol. 2023, 64, 222.

[46]	Z.Yang, F.Cao, H.Li, S.He, T.Zhao, H. Deng, J.Li, Z.Sun, C.Hao, J.Xu, Q.Guo, S.Liu, W. Guo, Acta Biomater. 2022, 150, 181.

[47]	Y.Gao, Q.Ma, Smart Med. 2022, 1, e20220012.

[48]	M.Afshar, G.Dini, S.Vaezifar, M. Mehdikhani, B.Movahedi, J. Drug Delivery Sci. Technol. 2020, 56, 101530.

[49]	M.Furtado, L.Chen, Z.Chen, A. Chen, W.Cui, Eng. Regen. 2022, 3, 217.

[50]	L.Li, J.Li, J.Guo, H. Zhang, X.Zhang, C.Yin, L.Wang, Y.Zhu, Q. Yao, Adv. Funct. Mater. 2019, 29, 1807356.

[51]	Z.Cai, Y.Tang, Y.Wei, P. Wang, H.Zhang, Acta Biomater. 2022, 152, 124.

[52]	F.Mohabatpour, A.Karkhaneh, A. M.Sharifi, RSC Adv. 2016, 6, 83135.

[53]	M. E.Prendergast, J. A. Burdick, Adv. Mater. 2020, 32, e1902516.

[54]	N.Yildirim, A.Amanzhanova, G.Kulzhanova, F.Mukasheva, C.Erisken, ACS Biomater. Sci. Eng. 2023, 9, 1205.

[55]	X.Zhu, Y.Xu, X.Xu, J.Zhu, L.Chen, Y. Xu, Y.Yang, N.Song, Small 2022, 18, e2201874.

[56]	J.Chen, Y.Li, S.Liu, Y. Du, S.Zhang, J.Wang, Acta Biomater. 2022, 154, 168.

[57]	D. K.Jeppesen, A. M.Fenix, J. L.Franklin, J. N.Higginbotham, Q. Zhang, L. J.Zimmerman, D. C.Liebler, J.Ping, Q.Liu, R. Evans, W. H.Fissell, J. G.Patton, L. H.Rome, D. T.Burnette, R. J.Coffey, Cell 2019, 177, 428.

[58]	M.Li, S.Li, C.Du, Y.Zhang, Y.Li, L.Chu, X.Han, H. Galons, Y.Zhang, H.Sun, P.Yu, Eur. J. Med. Chem. 2020, 207, 112784.

[59]	G. WonLee, M.Thangavelu, M.Joung Choi, E. YeongShin, H.Sol Kim, J. SeonBaek, Y.Woon Jeong, J. EunSong, C.Carlomagno, J.Miguel Oliveira, R. Luis Reis, G.Khang, J. Cell. Biochem. 2020, 121, 3642.

[60]	G.Mao, Z.Zhang, S.Hu, Z.Zhang, Z.Chang, Z. Huang, W.Liao, Y.Kang, Stem Cell Res. Ther. 2018, 9, 247.

[61]	J.Shao, J.Zhu, Y.Chen, Q. Fu, L.Li, Z.Ding, J.Wu, Y.Han, H. Li, Q.Qian, Y.Zhou, Stem Cells Int. 2021, 2021, 6624874.

[62]	F.Fagiani, D.Di Marino, A.Romagnoli, C.Travelli, D.Voltan, L. DiCesare Mannelli, M.Racchi, S.Govoni, C.Lanni, Signal. Transduct. Target. Ther. 2022, 7, 41.

[63]	M.Keshvari, M.Nejadtaghi, F.Hosseini-Beheshti, A.Rastqar, N.Patel, Chronobiol. Int. 2020, 37, 151.

[64]	C.Ke, H.Li, D.Yang, H. Ying, H.Zhu, J.Wang, J.Xu, L.Wang, Orthop. Surg. 2022, 14, 2230.

[65]	S. S.Tan, W.Zhan, C. J.Poon, X. Han, D.Marre, S.Boodhun, J. A.Palmer, G. M.Mitchell, W. A.Morrison, J. Tissue Eng. Regen. Med. 2018, 12, 382.

[66]	M. Y.Ha, D. H.Yang, S. J.You, H. J. Kim, H. J.Chun, NPJ Regen. Med. 2023, 8, 2.

[67]	Y. G.Kim, J.Choi, K.Kim, Biotechnol. J. 2020, 15, 2000082.

[68]	C.Bauer, E.Niculescu-Morzsa, V.Jeyakumar, D.Kern, S. S.Spath, S.Nehrer, J. Inflamm. 2016, 13, 31.

[69]	L.Li, G.Lv, B.Wang, L. Kuang, J. Cell. Physiol. 2020, 235, 281.

[70]	H.Zhang, D.Cai, X.Bai, Osteoarthritis Cartilage 2020, 28, 555.

[71]	K.Li, G.Yan, H.Huang, M. Zheng, K.Ma, X.Cui, D.Lu, L.Zheng, B. Zhu, J.Cheng, J.Zhao, J. Nanobiotechnol. 2022, 20, 38.

[72]	S.Zhang, S. J.Chuah, R. C.Lai, J. H. P. Hui, S. K.Lim, W. S.Toh, Biomaterials 2018, 156, 16.

RIGHTS & PERMISSIONS

2024 The Authors. View published by Shanghai Fuji Technology Consulting Co., Ltd, authorized by Professional Community of Experimental Medicine, National Association of Health Industry and Enterprise Management (PCEM) and John Wiley & Sons Australia, Ltd.