3D生物打印肝组织及其在外科中的应用前景_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

方致远 , 杨华瑜 ,  毛一雷

中国医学科学院北京协和医院肝脏外科（北京 100730）;

Corresponding author：

毛一雷, Email: pumch-liver@hotmail.com

Keywords：

DOI：

10.7507/1007-9424.202104004

Video：

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Citation： 方致远, 杨华瑜, 毛一雷. 3D生物打印肝组织及其在外科中的应用前景. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2021, 28(7): 846-849. doi: 10.7507/1007-9424.202104004 Copy

1.	Moroni L, Burdick JA, Highley C, et al. Biofabrication strategies for 3D in vitro models and regenerative medicine. Nat Rev Mater, 2018, 3(5): 21-37.
2.	Daly AC, Prendergast ME, Hughes AJ, et al. Bioprinting for the biologist. Cell, 2021, 184(1): 18-32.
3.	Ma L, Wu Y, Li Y, et al. Current advances on 3D-bioprinted liver tissue models. Adv Healthc Mater, 2020, 9(24): e2001517.
4.	Ozbolat IT, Hospodiuk M. Current advances and future perspectives in extrusion-based bioprinting. Biomaterials, 2016, 76: 321-343.
5.	Li X, Liu B, Pei B, et al. Inkjet bioprinting of biomaterials. Chem Rev, 2020, 120(19): 10793-10833.
6.	Kang HW, Lee SJ, Ko IK, et al. A 3D bioprinting system to produce human-scale tissue constructs with structural integrity. Nat Biotechnol, 2016, 34(3): 312-319.
7.	McCormack A, Highley CB, Leslie NR, et al. 3D printing in suspension baths: keeping the promises of bioprinting afloat. Trends Biotechnol, 2020, 38(6): 584-593.
8.	Lauschke VM, Vorrink SU, Moro SM, et al. Massive rearrangements of cellular MicroRNA signatures are key drivers of hepatocyte dedifferentiation. Hepatology, 2016, 64(5): 1743-1756.
9.	Nguyen DG, Funk J, Robbins JB, et al. Bioprinted 3D primary liver tissues allow assessment of organ-level response to clinical drug induced toxicity in vitro. PLoS One, 2016, 11(7): e0158674.
10.	Norona LM, Nguyen DG, Gerber DA, et al. Editor’s highlight: modeling compound-induced fibrogenesis in vitro using three-dimensional bioprinted human liver tissues. Toxicol Sci, 2016, 154(2): 354-367.
11.	Norona LM, Nguyen DG, Gerber DA, et al. Bioprinted liver provides early insight into the role of Kupffer cells in TGF-β1 and methotrexate-induced fibrogenesis. PLoS One, 2019, 14(1): e0208958.
12.	Castro RE, Diehl AM. Towards a definite mouse model of NAFLD. J Hepatol, 2018, 69(2): 272-274.
13.	Lee JW, Choi YJ, Yong WJ, et al. Development of a 3D cell printed construct considering angiogenesis for liver tissue engineering. Biofabrication, 2016, 8(1): 015007.
14.	Kim Y, Kang K, Jeong J, et al. Three-dimensional (3D) printing of mouse primary hepatocytes to generate 3D hepatic structure. Ann Surg Treat Res, 2017, 92(2): 67-72.
15.	Kim Y, Kang K, Yoon S, et al. Prolongation of liver-specific function for primary hepatocytes maintenance in 3D printed architectures. Organogenesis, 2018, 14(1): 1-12.
16.	Kim MK, Jeong W, Lee SM, et al. Decellularized extracellular matrix-based bio-ink with enhanced 3D printability and mechanical properties. Biofabrication, 2020, 12(2): 025003.
17.	Billiet T, Gevaert E, De Schryver T, et al. The 3D printing of gelatin methacrylamide cell-laden tissue-engineered constructs with high cell viability. Biomaterials, 2014, 35(1): 49-62.
18.	Jeon H, Kang K, Park SA, et al. Generation of multilayered 3D structures of HepG2 cells using a bio-printing technique. Gut Liver, 2017, 11(1): 121-128.
19.	Lee H, Han W, Kim H, et al. Development of liver decellularized extracellular matrix bioink for three-dimensional cell printing-based liver tissue engineering. Biomacromolecules, 2017, 18(4): 1229-1237.
20.	Massa S, Sakr MA, Seo J, et al. Bioprinted 3D vascularized tissue model for drug toxicity analysis. Biomicrofluidics, 2017, 11(4): 044109.
21.	Pimentel C R, Ko SK, Caviglia C, et al. Three-dimensional fabrication of thick and densely populated soft constructs with complex and actively perfused channel network. Acta Biomater, 2018, 65: 174-184.
22.	Wu Y, Wenger A, Golzar H, et al. 3D bioprinting of bicellular liver lobule-mimetic structures via microextrusion of cellulose nanocrystal-incorporated shear-thinning bioink. Sci Rep, 2020, 10(1): 20648.
23.	Kang D, Hong G, An S, et al. Bioprinting of multiscaled hepatic lobules within a highly vascularized construct. Small, 2020, 16(13): e1905505.
24.	Lewis PL, Green RM, Shah RN. 3D-printed gelatin scaffolds of differing pore geometry modulate hepatocyte function and gene expression. Acta Biomater, 2018, 69: 63-70.
25.	Hiller T, Berg J, Elomaa L, et al. Generation of a 3D liver model comprising human extracellular matrix in an alginate/gelatin-based bioink by extrusion bioprinting for infection and transduction studies. Int J Mol Sci, 2018, 19(10): 3129.
26.	Schmidt K, Berg J, Roehrs V, et al. 3D-bioprinted HepaRG cultures as a model for testing long term aflatoxin B1 toxicity in vitro. Toxicol Rep, 2020, 7: 1578-1587.
27.	Cuvellier M, Ezan F, Oliveira H, et al. 3D culture of HepaRG cells in GelMa and its application to bioprinting of a multicellular hepatic model. Biomaterials, 2021, 269: 120611.
28.	Yang H, Sun L, Pang Y, et al. Three-dimensional bioprinted hepatorganoids prolong survival of mice with liver failure. Gut, 2021, 70(3): 567-574.
29.	López-Terrada D, Cheung SW, Finegold MJ, et al. Hep G2 is a hepatoblastoma-derived cell line. Hum Pathol, 2009, 40(10): 1512-1515.
30.	Rowe C, Gerrard DT, Jenkins R, et al. Proteome-wide analyses of human hepatocytes during differentiation and dedifferentiation. Hepatology, 2013, 58(2): 799-809.
31.	Hart SN, Li Y, Nakamoto K, et al. A comparison of whole genome gene expression profiles of HepaRG cells and HepG2 cells to primary human hepatocytes and human liver tissues. Drug Metab Dispos, 2010, 38(6): 988-994.
32.	Lee JS, Yoon H, Yoon D, et al. Development of hepatic blocks using human adipose tissue-derived stem cells through three-dimensional cell printing techniques. J Mater Chem B, 2017, 5(5): 1098-1107.
33.	Kang K, Kim Y, Jeon H, et al. Three-dimensional bioprinting of hepatic structures with directly converted hepatocyte-like cells. Tissue Eng Part A, 2018, 24(7-8): 576-583.
34.	Baxter M, Withey S, Harrison S, et al. Phenotypic and functional analyses show stem cell-derived hepatocyte-like cells better mimic fetal rather than adult hepatocytes. J Hepatol, 2015, 62(3): 581-589.
35.	Huang P, Zhang L, Gao Y, et al. Direct reprogramming of human fibroblasts to functional and expandable hepatocytes. Cell Stem Cell, 2014, 14(3): 370-384.
36.	Ouyang L, Armstrong JPK, Chen Q, et al. Void-free 3D bioprinting for in-situ endothelialization and microfluidic perfusion. Adv Funct Mater, 2019, 30(1): 1908349.
37.	Mazzocchi A, Devarasetty M, Huntwork R, et al. Optimization of collagen type Ⅰ-hyaluronan hybrid bioink for 3D bioprinted liver microenvironments. Biofabrication, 2018, 11(1): 015003.
38.	Mao S, He J, Zhao Y, et al. Bioprinting of patient-derived in vitro intrahepatic cholangiocarcinoma tumor model: establishment, evaluation and anti-cancer drug testing. Biofabrication, 2020, 12(4): 045014.
39.	Sun L, Yang H, Wang Y, et al. Application of a 3D bioprinted hepatocellular carcinoma cell model in antitumor drug research. Front Oncol, 2020, 10: 878.
40.	Xie F, Sun L, Pang Y, et al. Three-dimensional bio-printing of primary human hepatocellular carcinoma for personalized medicine. Biomaterials, 2021, 265: 120416.
41.	Lim KS, Galarraga JH, Cui X, et al. Fundamentals and applications of photo-cross-linking in bioprinting. Chem Rev, 2020, 120(19): 10662-10694.
42.	Ma X, Qu X, Zhu W, et al. Deterministically patterned biomimetic human iPSC-derived hepatic model via rapid 3D bioprinting. Proc Natl Acad Sci U S A, 2016, 113(8): 2206-2211.
43.	Mao Q, Wang Y, Li Y, et al. Fabrication of liver microtissue with liver decellularized extracellular matrix (dECM) bioink by digital light processing (DLP) bioprinting. Mater Sci Eng C Mater Biol Appl, 2020, 109: 110625.
44.	Ong CS, Fukunishi T, Zhang H, et al. Biomaterial-free three-dimensional bioprinting of cardiac tissue using human induced pluripotent stem cell derived cardiomyocytes. Sci Rep, 2017, 7(1): 4566.
45.	Ayan B, Heo DN, Zhang Z, et al. Aspiration-assisted bioprinting for precise positioning of biologics. Sci Adv, 2020, 6(10): eaaw5111.
46.	Kizawa H, Nagao E, Shimamura M, et al. Scaffold-free 3D bio-printed human liver tissue stably maintains metabolic functions useful for drug discovery. Biochem Biophys Rep, 2017, 10: 186-191.
47.	Yanagi Y, Nakayama K, Taguchi T, et al. In vivo and ex vivo methods of growing a liver bud through tissue connection. Sci Rep, 2017, 7(1): 14085.
48.	Chang R, Emami K, Wu H, et al. Biofabrication of a three-dimensional liver micro-organ as an in vitro drug metabolism model. Biofabrication, 2010, 2(4): 045004.
49.	Snyder JE, Hamid Q, Wang C, et al. Bioprinting cell-laden matrigel for radioprotection study of liver by pro-drug conversion in a dual-tissue microfluidic chip. Biofabrication, 2011, 3(3): 034112.
50.	Bhise NS, Manoharan V, Massa S, et al. A liver-on-a-chip platform with bioprinted hepatic spheroids. Biofabrication, 2016, 8(1): 014101.
51.	Lee H, Cho DW. One-step fabrication of an organ-on-a-chip with spatial heterogeneity using a 3D bioprinting technology. Lab Chip, 2016, 16(14): 2618-2625.
52.	Grix T, Ruppelt A, Thomas A, et al. Bioprinting perfusion-enabled liver equivalents for advanced organ-on-a-chip applications. Genes (Basel), 2018, 9(4): 176.
53.	Lee H, Chae S, Kim JY, et al. Cell-printed 3D liver-on-a-chip possessing a liver microenvironment and biliary system. Biofabrication, 2019, 11(2): 025001.
54.	Lee H, Kim J, Choi Y, et al. Application of gelatin bioinks and cell-printing technology to enhance cell delivery capability for 3D liver fibrosis-on-a-chip development. ACS Biomater Sci Eng, 2020, 6(4): 2469-2477.

1. Moroni L, Burdick JA, Highley C, et al. Biofabrication strategies for 3D in vitro models and regenerative medicine. Nat Rev Mater, 2018, 3(5): 21-37.
2. Daly AC, Prendergast ME, Hughes AJ, et al. Bioprinting for the biologist. Cell, 2021, 184(1): 18-32.
3. Ma L, Wu Y, Li Y, et al. Current advances on 3D-bioprinted liver tissue models. Adv Healthc Mater, 2020, 9(24): e2001517.
4. Ozbolat IT, Hospodiuk M. Current advances and future perspectives in extrusion-based bioprinting. Biomaterials, 2016, 76: 321-343.
5. Li X, Liu B, Pei B, et al. Inkjet bioprinting of biomaterials. Chem Rev, 2020, 120(19): 10793-10833.
6. Kang HW, Lee SJ, Ko IK, et al. A 3D bioprinting system to produce human-scale tissue constructs with structural integrity. Nat Biotechnol, 2016, 34(3): 312-319.
7. McCormack A, Highley CB, Leslie NR, et al. 3D printing in suspension baths: keeping the promises of bioprinting afloat. Trends Biotechnol, 2020, 38(6): 584-593.
8. Lauschke VM, Vorrink SU, Moro SM, et al. Massive rearrangements of cellular MicroRNA signatures are key drivers of hepatocyte dedifferentiation. Hepatology, 2016, 64(5): 1743-1756.
9. Nguyen DG, Funk J, Robbins JB, et al. Bioprinted 3D primary liver tissues allow assessment of organ-level response to clinical drug induced toxicity in vitro. PLoS One, 2016, 11(7): e0158674.
10. Norona LM, Nguyen DG, Gerber DA, et al. Editor’s highlight: modeling compound-induced fibrogenesis in vitro using three-dimensional bioprinted human liver tissues. Toxicol Sci, 2016, 154(2): 354-367.
11. Norona LM, Nguyen DG, Gerber DA, et al. Bioprinted liver provides early insight into the role of Kupffer cells in TGF-β1 and methotrexate-induced fibrogenesis. PLoS One, 2019, 14(1): e0208958.
12. Castro RE, Diehl AM. Towards a definite mouse model of NAFLD. J Hepatol, 2018, 69(2): 272-274.
13. Lee JW, Choi YJ, Yong WJ, et al. Development of a 3D cell printed construct considering angiogenesis for liver tissue engineering. Biofabrication, 2016, 8(1): 015007.
14. Kim Y, Kang K, Jeong J, et al. Three-dimensional (3D) printing of mouse primary hepatocytes to generate 3D hepatic structure. Ann Surg Treat Res, 2017, 92(2): 67-72.
15. Kim Y, Kang K, Yoon S, et al. Prolongation of liver-specific function for primary hepatocytes maintenance in 3D printed architectures. Organogenesis, 2018, 14(1): 1-12.
16. Kim MK, Jeong W, Lee SM, et al. Decellularized extracellular matrix-based bio-ink with enhanced 3D printability and mechanical properties. Biofabrication, 2020, 12(2): 025003.
17. Billiet T, Gevaert E, De Schryver T, et al. The 3D printing of gelatin methacrylamide cell-laden tissue-engineered constructs with high cell viability. Biomaterials, 2014, 35(1): 49-62.
18. Jeon H, Kang K, Park SA, et al. Generation of multilayered 3D structures of HepG2 cells using a bio-printing technique. Gut Liver, 2017, 11(1): 121-128.
19. Lee H, Han W, Kim H, et al. Development of liver decellularized extracellular matrix bioink for three-dimensional cell printing-based liver tissue engineering. Biomacromolecules, 2017, 18(4): 1229-1237.
20. Massa S, Sakr MA, Seo J, et al. Bioprinted 3D vascularized tissue model for drug toxicity analysis. Biomicrofluidics, 2017, 11(4): 044109.
21. Pimentel C R, Ko SK, Caviglia C, et al. Three-dimensional fabrication of thick and densely populated soft constructs with complex and actively perfused channel network. Acta Biomater, 2018, 65: 174-184.
22. Wu Y, Wenger A, Golzar H, et al. 3D bioprinting of bicellular liver lobule-mimetic structures via microextrusion of cellulose nanocrystal-incorporated shear-thinning bioink. Sci Rep, 2020, 10(1): 20648.
23. Kang D, Hong G, An S, et al. Bioprinting of multiscaled hepatic lobules within a highly vascularized construct. Small, 2020, 16(13): e1905505.
24. Lewis PL, Green RM, Shah RN. 3D-printed gelatin scaffolds of differing pore geometry modulate hepatocyte function and gene expression. Acta Biomater, 2018, 69: 63-70.
25. Hiller T, Berg J, Elomaa L, et al. Generation of a 3D liver model comprising human extracellular matrix in an alginate/gelatin-based bioink by extrusion bioprinting for infection and transduction studies. Int J Mol Sci, 2018, 19(10): 3129.
26. Schmidt K, Berg J, Roehrs V, et al. 3D-bioprinted HepaRG cultures as a model for testing long term aflatoxin B1 toxicity in vitro. Toxicol Rep, 2020, 7: 1578-1587.
27. Cuvellier M, Ezan F, Oliveira H, et al. 3D culture of HepaRG cells in GelMa and its application to bioprinting of a multicellular hepatic model. Biomaterials, 2021, 269: 120611.
28. Yang H, Sun L, Pang Y, et al. Three-dimensional bioprinted hepatorganoids prolong survival of mice with liver failure. Gut, 2021, 70(3): 567-574.
29. López-Terrada D, Cheung SW, Finegold MJ, et al. Hep G2 is a hepatoblastoma-derived cell line. Hum Pathol, 2009, 40(10): 1512-1515.
30. Rowe C, Gerrard DT, Jenkins R, et al. Proteome-wide analyses of human hepatocytes during differentiation and dedifferentiation. Hepatology, 2013, 58(2): 799-809.
31. Hart SN, Li Y, Nakamoto K, et al. A comparison of whole genome gene expression profiles of HepaRG cells and HepG2 cells to primary human hepatocytes and human liver tissues. Drug Metab Dispos, 2010, 38(6): 988-994.
32. Lee JS, Yoon H, Yoon D, et al. Development of hepatic blocks using human adipose tissue-derived stem cells through three-dimensional cell printing techniques. J Mater Chem B, 2017, 5(5): 1098-1107.
33. Kang K, Kim Y, Jeon H, et al. Three-dimensional bioprinting of hepatic structures with directly converted hepatocyte-like cells. Tissue Eng Part A, 2018, 24(7-8): 576-583.
34. Baxter M, Withey S, Harrison S, et al. Phenotypic and functional analyses show stem cell-derived hepatocyte-like cells better mimic fetal rather than adult hepatocytes. J Hepatol, 2015, 62(3): 581-589.
35. Huang P, Zhang L, Gao Y, et al. Direct reprogramming of human fibroblasts to functional and expandable hepatocytes. Cell Stem Cell, 2014, 14(3): 370-384.
36. Ouyang L, Armstrong JPK, Chen Q, et al. Void-free 3D bioprinting for in-situ endothelialization and microfluidic perfusion. Adv Funct Mater, 2019, 30(1): 1908349.
37. Mazzocchi A, Devarasetty M, Huntwork R, et al. Optimization of collagen type Ⅰ-hyaluronan hybrid bioink for 3D bioprinted liver microenvironments. Biofabrication, 2018, 11(1): 015003.
38. Mao S, He J, Zhao Y, et al. Bioprinting of patient-derived in vitro intrahepatic cholangiocarcinoma tumor model: establishment, evaluation and anti-cancer drug testing. Biofabrication, 2020, 12(4): 045014.
39. Sun L, Yang H, Wang Y, et al. Application of a 3D bioprinted hepatocellular carcinoma cell model in antitumor drug research. Front Oncol, 2020, 10: 878.
40. Xie F, Sun L, Pang Y, et al. Three-dimensional bio-printing of primary human hepatocellular carcinoma for personalized medicine. Biomaterials, 2021, 265: 120416.
41. Lim KS, Galarraga JH, Cui X, et al. Fundamentals and applications of photo-cross-linking in bioprinting. Chem Rev, 2020, 120(19): 10662-10694.
42. Ma X, Qu X, Zhu W, et al. Deterministically patterned biomimetic human iPSC-derived hepatic model via rapid 3D bioprinting. Proc Natl Acad Sci U S A, 2016, 113(8): 2206-2211.
43. Mao Q, Wang Y, Li Y, et al. Fabrication of liver microtissue with liver decellularized extracellular matrix (dECM) bioink by digital light processing (DLP) bioprinting. Mater Sci Eng C Mater Biol Appl, 2020, 109: 110625.
44. Ong CS, Fukunishi T, Zhang H, et al. Biomaterial-free three-dimensional bioprinting of cardiac tissue using human induced pluripotent stem cell derived cardiomyocytes. Sci Rep, 2017, 7(1): 4566.
45. Ayan B, Heo DN, Zhang Z, et al. Aspiration-assisted bioprinting for precise positioning of biologics. Sci Adv, 2020, 6(10): eaaw5111.
46. Kizawa H, Nagao E, Shimamura M, et al. Scaffold-free 3D bio-printed human liver tissue stably maintains metabolic functions useful for drug discovery. Biochem Biophys Rep, 2017, 10: 186-191.
47. Yanagi Y, Nakayama K, Taguchi T, et al. In vivo and ex vivo methods of growing a liver bud through tissue connection. Sci Rep, 2017, 7(1): 14085.
48. Chang R, Emami K, Wu H, et al. Biofabrication of a three-dimensional liver micro-organ as an in vitro drug metabolism model. Biofabrication, 2010, 2(4): 045004.
49. Snyder JE, Hamid Q, Wang C, et al. Bioprinting cell-laden matrigel for radioprotection study of liver by pro-drug conversion in a dual-tissue microfluidic chip. Biofabrication, 2011, 3(3): 034112.
50. Bhise NS, Manoharan V, Massa S, et al. A liver-on-a-chip platform with bioprinted hepatic spheroids. Biofabrication, 2016, 8(1): 014101.
51. Lee H, Cho DW. One-step fabrication of an organ-on-a-chip with spatial heterogeneity using a 3D bioprinting technology. Lab Chip, 2016, 16(14): 2618-2625.
52. Grix T, Ruppelt A, Thomas A, et al. Bioprinting perfusion-enabled liver equivalents for advanced organ-on-a-chip applications. Genes (Basel), 2018, 9(4): 176.
53. Lee H, Chae S, Kim JY, et al. Cell-printed 3D liver-on-a-chip possessing a liver microenvironment and biliary system. Biofabrication, 2019, 11(2): 025001.
54. Lee H, Kim J, Choi Y, et al. Application of gelatin bioinks and cell-printing technology to enhance cell delivery capability for 3D liver fibrosis-on-a-chip development. ACS Biomater Sci Eng, 2020, 6(4): 2469-2477.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

3D生物打印肝组织及其在外科中的应用前景

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