Abstract
Bioprinting has been a flouring way to fabricate complex tissue and organ mimics via precisely depositing printable cell-laden biomaterials. However, there is a limited number of biomaterials that fulfill the mechanical property of printing while meeting the responsive environment desired for the cells. Despite excellent cell compatibility and bioactivity, collagen suffers from difficulties in processing and printability which inhibited its utilization in three-dimensional (3D) bioprinting. Herein, we address this limitation by using ionic liquid as the solvent in the modification process, enabling collagens modified with quantified norbornene for chemical crosslink and extrusion-based 3D printing. With improved solubility and rheological properties, norbornene-functionalized collagen (Col-Nor) exhibited better shape fidelity in extrusion-based 3D printing compared with the one before modification. Photo-crosslinked Col-Nor hydrogel provided structural support and promoted the adhesion, proliferation, and differentiation of various types of cells, which afforded a centimeter-scale liver tissue model. This highly generalizable methodology expands printable, versatile, and tunable hydrogels developed from the natural extracellular matrix, allowing the biofabrication of 3D liver tissue model with branched vascular networks.
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References
Hofer M, Lutolf MP. Nat Rev Mater, 2021, 6: 402–420
Takebe T, Wells JM. Science, 2019, 364: 956–959
Dekkers JF, van Vliet EJ, Sachs N, Rosenbluth JM, Kopper O, Rebel HG, Wehrens EJ, Piani C, Visvader JE, Verissimo CS, Boj SF, Brugge JS, Clevers H, Rios AC. Nat Protoc, 2021, 16: 1936–1965
Broutier L, Mastrogiovanni G, Verstegen MM, Francies HE, Gavarró LM, Bradshaw CR, Allen GE, Arnes-Benito R, Sidorova O, Gaspersz MP, Georgakopoulos N, Koo BK, Dietmann S, Davies SE, Praseedom RK, Lieshout R, IJzermans JNM, Wigmore SJ, Saeb-Parsy K, Garnett MJ, van der Laan LJ, Huch M. Nat Med, 2017, 23: 1424–1435
Mukhopadhyay M. Nat Methods, 2021, 18: 596
Fyfe I. Nat Rev Neurol, 2021, 17: 1
Li X, Liu B, Pei B, Chen J, Zhou D, Peng J, Zhang X, Jia W, Xu T. Chem Rev, 2020, 120: 10793–10833
Ng WL, Lee JM, Zhou M, Chen YW, Lee KXA, Yeong WY, Shen YF. Biofabrication, 2020, 12: 022001
Jiang T, Munguia-Lopez JG, Flores-Torres S, Kort-Mascort J, Kinsella JM. Appl Phys Rev, 2019, 6: 011310
Murphy SV, Atala A. Nat Biotechnol, 2014, 32: 773–785
Jungst T, Smolan W, Schacht K, Scheibel T, Groll J. Chem Rev, 2016, 116: 1496–1539
Bedell ML, Navara AM, Du Y, Zhang S, Mikos AG. Chem Rev, 2020, 120: 10744–10792
Chen WH, Chen QW, Chen Q, Cui C, Duan S, Kang Y, Liu Y, Liu Y, Muhammad W, Shao S, Tang C, Wang J, Wang L, Xiong MH, Yin L, Zhang K, Zhang Z, Zhen X, Feng J, Gao C, Gu Z, He C, Ji J, Jiang X, Liu W, Liu Z, Peng H, Shen Y, Shi L, Sun X, Wang H, Wang J, Xiao H, Xu FJ, Zhong Z, Zhang XZ, Chen X. Sci China Chem, 2022, 65: 1010–1075
Karsdal MA, Nielsen SH, Leeming DJ, Langholm LL, Nielsen MJ, Manon-Jensen T, Siebuhr A, Gudmann NS, Rønnow S, Sand JM, Daniels SJ, Mortensen JH, Schuppan D. Adv Drug Deliver Rev, 2017, 121: 43–56
Bielajew BJ, Hu JC, Athanasiou KA. Nat Rev Mater, 2020, 5: 730–747
Wang Y, Yuan J, Zhao Y, Wang L, Guo L, Feng L, Cui J, Dong S, Wan S, Liu W, Hoffmann H, Tieu K, Hao J. CCS Chem, 2021, 4: 2102–2114
Frantz C, Stewart KM, Weaver VM. J Cell Sci, 2010, 123: 4195–4200
Rong Y, Zhang Z, He C, Chen X. Sci China Chem, 2020, 63: 1100–1111
Yang Q, Lv X, Gao B, Ji Y, Xu F. Adv Appl Mech, 2021, 54: 285–318
Olegovich Osidak E, Igorevich Kozhukhov V, Sergeevna Osidak M, Petrovich Domogatskiy S. Int J Bioprint, 2020, 6: 270
Yu R, Li Z, Pan G, Guo B. Sci China Chem, 2022, 65: 2238–2251
Gu L, Shan T, Ma Y, Tay FR, Niu L. Trends Biotechnol, 2019, 37: 464–491
Tanzer ML. Science, 1973, 180: 561–566
Sorushanova A, Delgado LM, Wu Z, Shologu N, Kshirsagar A, Raghunath R, Mullen AM, Bayon Y, Pandit A, Raghunath M, Zeugolis DI. Adv Mater, 2019, 31: 1801651
Duarte Campos DF, Blaeser A, Korsten A, Neuss S, Jäkel J, Vogt M, Fischer H. Tissue Eng Part A, 2015, 21: 740–756
Atala A. Chem Rev, 2020, 120: 10545–10546
Zhao X, Song W, Liu S, Ren L. Sci China Chem, 2016, 59: 1548–1553
Lee JM, Suen SKQ, Ng WL, Ma WC, Yeong WY. Macromol Biosci, 2021, 21: 2000280
Zhong L, Qu Y, Shi K, Chu B, Lei M, Huang K, Gu Y, Qian Z. Sci China Chem, 2018, 61: 1553–1567
Nerger BA, Brun PT, Nelson CM. Soft Matter, 2019, 15: 5728–5738
Stratesteffen H, Köpf M, Kreimendahl F, Blaeser A, Jockenhoevel S, Fischer H. Biofabrication, 2017, 9: 045002
Hull SM, Lindsay CD, Brunel LG, Shiwarski DJ, Tashman JW, Roth JG, Myung D, Feinberg AW, Heilshorn SC. Adv Funct Mater, 2021, 31: 2007983
Szklanny AA, Machour M, Redenski I, Chochola V, Goldfracht I, Kaplan B, Epshtein M, Simaan Yameen H, Merdler U, Feinberg A, Seliktar D, Korin N, Jaroš J, Levenberg S. Adv Mater, 2021, 33: 2102661
Guo K, Wang H, Li S, Zhang H, Li S, Zhu H, Yang Z, Zhang L, Chang P, Zheng X. ACS Appl Mater Interfaces, 2021, 13: 7037–7050
Lee A, Hudson AR, Shiwarski DJ, Tashman JW, Hinton TJ, Yerneni S, Bliley JM, Campbell PG, Feinberg AW. Science, 2019, 365: 482–487
Hull SM, Brunel LG, Heilshorn SC. Adv Mater, 2022, 34: 2103691
Ouyang L, Highley CB, Sun W, Burdick JA. Adv Mater, 2017, 29: 1604983
Ding S, Hülsey MJ, An H, He Q, Asakura H, Gao M, Hasegawa J, Tanaka T, Yan N. CCS Chem, 2021, 3: 1814–1822
Long JX, Li XH, Wang LF, Zhang N. Sci China Chem, 2012, 55: 1500–1508
Wang B, Qin L, Mu T, Xue Z, Gao G. Chem Rev, 2017, 117: 7113–7131
Mahmood H, Moniruzzaman M, Yusup S, Welton T. Green Chem, 2017, 19: 2051–2075
Wang H, Gurau G, Rogers RD. Chem Soc Rev, 2012, 41: 1519–1537
Meng Z, Zheng X, Tang K, Liu J, Ma Z, Zhao Q. Int J Biol Macromolecules, 2012, 51: 440–448
Iqbal B, Muhammad N, Jamal A, Ahmad P, Khan ZUH, Rahim A, Khan AS, Gonfa G, Iqbal J, Rehman IU. J Mol Liquids, 2017, 243: 720–725
Wang J, Wei L, Ma Y, Li K, Li M, Yu Y, Wang L, Qiu H. Carbohyd Polym, 2013, 98: 736–743
Zhao H, Xu J, Yuan H, Zhang E, Dai N, Gao Z, Huang Y, Lv F, Liu L, Gu Q, Wang S. Mater Horiz, 2022, 9: 342–349
Zhao H, Xu J, Zhang E, Qi R, Huang Y, Lv F, Liu L, Gu Q, Wang S. ACS Appl Mater Interfaces, 2021, 13: 25759–25770
Liu X, Wang X, Zhang L, Sun L, Wang H, Zhao H, Zhang Z, Liu W, Huang Y, Ji S, Zhang J, Li K, Song B, Li C, Zhang H, Li S, Wang S, Zheng X, Gu Q. Adv Healthcare Mater, 2021, 10: 2101405
Mehta A, Rao JR, Fathima NN. Colloids Surfs B-Biointerfaces, 2014, 117: 376–382
Valot L, Martinez J, Mehdi A, Subra G. Chem Soc Rev, 2019, 48: 4049–4086
Oosterlaken BM, Vena MP, With G. Adv Mater, 2021, 33: 2004418
Suehiro T, Kojima C, Tsumura S, Harada A, Kono K. Biopolymers, 2010, 93: 640–648
Liu W, Heinrich MA, Zhou Y, Akpek A, Hu N, Liu X, Guan X, Zhong Z, Jin X, Khademhosseini A, Zhang YS. Adv Healthcare Mater, 2017, 6: 1601451
Ouyang L, Yao R, Zhao Y, Sun W. Biofabrication, 2016, 8: 035020
Li H, Tan C, Li L. Mater Des, 2018, 159: 20–38
Unagolla JM, Jayasuriya AC. Appl Mater Today, 2020, 18: 100479
Bernal W, Jalan R, Quaglia A, Simpson K, Wendon J, Burroughs A. Lancet, 2015, 386: 1576–1587
Fisher RA. Nat Rev Gastroenterol Hepatol, 2017, 14: 373–382
Bogdanos DP, Gao B, Gershwin ME. Compr Physiol, 2013, 3: 567–598
Acknowledgements
This work was supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA16020804, XDA16020802) and the National Natural Science Foundation of China (22021002, 22022705). We are grateful to the research group of Prof. Lijian Hui for the help with HUVEC and PHH cells.
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Synthesis of easily-processable collagen bio-inks using ionic liquid for 3D bioprinted liver tissue models with branched vascular networks
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Gao, Z., Liu, X., Zhao, H. et al. Synthesis of easily-processable collagen bio-inks using ionic liquid for 3D bioprinted liver tissue models with branched vascular networks. Sci. China Chem. 66, 1489–1499 (2023). https://doi.org/10.1007/s11426-022-1472-6
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DOI: https://doi.org/10.1007/s11426-022-1472-6