Research progress of shear-thinned biological ink in 3D bioprinting tissue trachea_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

SUN Yiqi ^1,2,3 , XV Xiangyu ^1,2,3 , SUN Fei ^1,2,3 , SHAN Yibo ^1,2,3 , SHEN Zhiming ^1,2,3 ,  SHI Hongcan ^1,2,3

1. Clinical Medical College, Yangzhou University, Yangzhou, 225009, P. R. China;
2. Institute of Translational Medicine, Medical College, Yangzhou University, Yangzhou, 225009, Jiangshu, P. R. China;
3. Jiangsu Key Laboratory of Integrated Traditional Chinese and Western Medicine for Prevention and Treatment of Senile Diseases, Yangzhou University, Yangzhou 225009, Jiangshu, P. R. China;

Corresponding author：

SHI Hongcan, Email: shihongcan@163.com

Keywords：

Shear thinning; bioink; tracheal graft; tissue engineering; 3D printing

DOI：

10.7507/1007-4848.202301039

Video：

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Abstract Full text Figures/Tables Video References Cited by

Shear thinning is an ideal feature of biological ink because it can reduce the chance of blocking. For extrusion based biological printing, biological ink will experience shear force when passing through the biological printer. The shear rate will increase with the increase of extrusion rate, and the apparent viscosity of shear thinning bio-ink will decrease, which makes it easier to block, thus achieving the structural fidelity of 3D printing tissue. The manufacturing of complex functional structures in tissue trachea requires the precise placement and coagulation of biological ink layer by layer, and the shear-thinning biological ink may well meet this requirement. This review focuses on the importance of mechanical properties, classification and preparation methods of shear-thinning biological ink, and lists its current application status in 3D printing tissue trachea to discuss the more possibilities and prospects of this biological material in tissue trachea.

1.	Choudhury D, Tun HW, Wang T, et al. Organ-derived decellularized extracellular matrix: A game changer for bioink manufacturing? Trends Biotechnol, 2018 Aug;36(8): 787-805.
2.	Rock JR, Randell SH, Hogan BL. Airway basal stem cells: A perspective on their roles in epithelial homeostasis and remodeling. Dis Model Mech, 2010, 3(9-10): 545-556.
3.	Li N, Guo R, Zhang ZJ. Bioink formulations for bone tissue regeneration. Front Bioeng Biotechnol, 2021, 9: 630488.
4.	Zhang YS, Yue K, Aleman J, et al. 3D Bioprinting for tissue and organ fabrication. Ann Biomed Eng, 2017, 45(1): 148-163.
5.	Jungst T, Smolan W, Schacht K, et al. Strategies and molecular design criteria for 3D printable hydrogels. Chem Rev, 2016, 116(3): 1496-539.
6.	Garcia-Cruz MR, Postma A, Frith JE, et al. Printability and bio-functionality of a shear thinning methacrylated xanthan-gelatin composite bioink. Biofabrication, 2021, 13(3):doi: 10.1088/1758-5090/abec2d. .
7.	Mörö A, Samanta S, Honkamäki L, et al. Hyaluronic acid based next generation bioink for 3D bioprinting of human stem cell derived corneal stromal model with innervation. Biofabrication, 2022, 15(1) :doi: 10.1088/1758-5090/acab34.
8.	Shams E, Barzad MS, Mohamadnia S, et al. A review on alginate-based bioinks, combination with other natural biomaterials and characteristics. J Biomater Appl, 2022, 37(2): 355-372.
9.	Blaeser A, Duarte Campos DF, Puster U, et al. Controlling shear stress in 3d bioprinting is a key factor to balance printing resolution and stem cell integrity. Adv Healthc Mater, 2016, 5(3): 326-333.
10.	Liu W, Heinrich MA, Zhou Y, et al. Extrusion Bioprinting of Shear-Thinning Gelatin Methacryloyl Bioinks. Adv Healthc Mater, 2017, 6(12): 10.1002/adhm. 201601451.
11.	Poldervaart MT, Goversen B, de Ruijter M, et al. 3D bioprinting of methacrylated hyaluronic acid (MeHA) hydrogel with intrinsic osteogenicity. PLoS One, 2017, 12(6): e0177628.
12.	Gomez-Florit M, Pardo A, Domingues RMA, et al. Natural-based hydrogels for tissue engineering applications. Molecules, 2020, 25(24): 5858.
13.	Decante G, Costa JB, Silva-Correia J, et al. Engineering bioinks for 3D bioprinting. Biofabrication, 2021, 13(3).
14.	Heinrich MA, Liu W, Jimenez A, et al. 3D Bioprinting: From benches to translational applications. Small, 2019, 15(23): e1805510.
15.	Wang Z, Zhang Y, Yin Y, et al. High-strength and injectable supramolecular ion wound hhydrogel self-assembled by monomeric nucleoside for tooth-extractealing. Adv Mater, 2022, 34(13): e2108300.
16.	Cha GD, Lee WH, Sunwoo SH, et al. Multifunctional injectable hydrogel for in vivo diagnostic and therapeutic applications. ACS Nano, 2022, 16(1): 554-556.
17.	Freeman S, Calabro S, Williams R, et al. Bioink formulation and machine learning-empowered bioprinting optimization. Front Bioeng Biotechnol, 2022,doi: 10.3389/fbioe.2022.913579. .
18.	Shin M, Galarraga JH, Kwon MY, et al. Gallol-derived ECM-mimetic adhesive bioinks exhibiting temporal shear-thinning and stabilization behavior. Acta Biomater, 2019, 95: 165-175.
19.	Gungor-Ozkerim PS, Inci I, Zhang YS, et al. Bioinks for 3D bioprinting: an overview. Biomater Sci, 2018, 6(5): 915-946.
20.	Moeinzadeh S, Park Y, Lin S, et al. In-situ stable injectable collagen-based hydrogels for cell and growth factor delivery. Materialia (Oxf), 2021,doi: 10.1016/j.mtla.2020.100954.
21.	Stratesteffen H, Köpf M, Kreimendahl F, et al. GelMA-collagen blends enable drop-on-demand 3D printablility and promote angiogenesis. Biofabrication, 2017, 9(4): 045002.
22.	Leucht A, Volz AC, Rogal J, et al. Advanced gelatin-based vascularization bioinks for extrusion-based bioprinting of vascularized bone equivalents. Sci Rep, 2020, 10(1): 5330.
23.	McBeth C, Lauer J, Ottersbach M, et al. 3D bioprinting of GelMA scaffolds triggers mineral deposition by primary human osteoblasts. Biofabrication, 2017, 9(1): 015009.
24.	Behan K, Dufour A, Garcia O, et al. Methacrylated Cartilage ECM-based hydrogels as injectables and bioinks for cartilage tissue engineering. Biomolecules, 2022, 12(2): 216.
25.	Kim BS, Kim H, Gao G, et al. Decellularized extracellular matrix: A step towards the next generation source for bioink manufacturing. Biofabrication, 2017, 9(3): 034104.
26.	De Santis MM, Alsafadi HN, Tas S, et al. Extracellular-matrix-reinforced bioinks for 3D bioprinting human tissue. Adv Mater, 2021, 33(3): e2005476.
27.	Chimene D, Kaunas R, Gaharwar AK. Hydrogel bioink reinforcement for additive manufacturing: A focused review of emerging strategies. Adv Mater, 2020, 32(1): e1902026.
28.	Dubbin K, Tabet A, Heilshorn SC. Quantitative criteria to benchmark new and existing bio-inks for cell compatibility. Biofabrication, 2017, 9(4): 044102.
29.	Abdulghani S, Morouço PG. Biofabrication for osteochondral tissue regeneration: Bioink printability requirements. J Mater Sci Mater Med, 2019, 30(2): 20.
30.	Matai I, Kaur G, Seyedsalehi A, et al. Progress in 3D bioprinting technology for tissue/organ regenerative engineering. Biomaterials, 2020, 226: 119536.
31.	Panda S, Hajra S, Mistewicz K, et al. A focused review on three-dimensional bioprinting technology for artificial organ fabrication. Biomater Sci, 2022, 10(18): 5054-5080.
32.	Boscher J, Gachet C, Lanza F, et al. Megakaryocyte culture in 3D methylcellulose-based hydrogel to improve cell maturation and study the impact of stiffness and confinement. J Vis Exp, 2021, (174). doi: 10.3791/62511.
33.	Jiang J, Woulfe DS, Papoutsakis ET. Shear enhances thrombopoiesis and formation of microparticles that induce megakaryocytic differentiation of stem cells. Blood, 2014, 124(13): 2094-2103.
34.	Duarte Campos DF, Blaeser A, Weber M, et al. Three-dimensional printing of stem cell-laden hydrogels submerged in a hydrophobic high-density fluid. Biofabrication, 2013, 5(1): 015003.
35.	Duraj-Thatte AM, Manjula-Basavanna A, Rutledge J, et al. Programmable microbial ink for 3D printing of living materials produced from genetically engineered protein nanofibers. Nat Commun, 2021, 12(1): 6600.
36.	Duraj-Thatte AM, Courchesne ND, Praveschotinunt P, et al. Genetically programmable self-regenerating bacterial hydrogels. Adv Mater, 2019, 31(40): e1901826.
37.	Yan Z, Yin M, Chen J, et al. Assembly and substrate recognition of curli biogenesis system. Nat Commun, 2020, 11(1): 241.
38.	Zandi N, Sani ES, Mostafavi E, et al. Nanoengineered shear-thinning and bioprintable hydrogel as a versatile platform for biomedical applications. Biomaterials, 2021, 267: 120476.
39.	Nojoomi A, Tamjid E, Simchi A, et al. Injectable polyethylene glycol-laponite composite hydrogels as articular cartilage scaffolds with superior mechanical and rheological properties. Intern J Polym Mater Polym Biomater, 2017, 66(3): 105-114.
40.	Ding X, Gao J, Awada H, et al. Dual physical dynamic bond-based injectable and biodegradable hydrogel for tissue regeneration. J Mater Chem B, 2016, 4(6): 1175-1185.
41.	Ren X, Zhou Q, Foulad D, et al. Nanoparticulate mineralized collagen glycosaminoglycan materials directly and indirectly inhibit osteoclastogenesis and osteoclast activation. J Tissue Eng Regen Med, 2019, 13(5): 823-834.
42.	Barisón MJ, Nogoceke R, Josino R, et al. Functionalized hydrogels for cartilage repair: The value of secretome-instructive signaling. Int J Mol Sci, 2022, 23(11): 6010.
43.	Im S, Choe G, Seok JM, et al. An osteogenic bioink composed of alginate, cellulose nanofibrils, and polydopamine nanoparticles for 3D bioprinting and bone tissue engineering. Int J Biol Macromol, 2022, 205: 520-529.
44.	Markstedt K, Mantas A, Tournier I, et al. 3D Bioprinting human chondrocytes with nanocellulose-alginate bioink for cartilage tissue engineering applications. Biomacromolecules, 2015, 16(5): 1489-1496.
45.	Freeman S, Calabro S, Williams R, et al. Bioink formulation and machine learning-empowered bioprinting optimization. Front Bioeng Biotechnol, 2022, 10: 913579.
46.	Chen Y, Xiong X, Liu X, et al. 3D Bioprinting of shear-thinning hybrid bioinks with excellent bioactivity derived from gellan/alginate and thixotropic magnesium phosphate-based gels. J Mater Chem B, 2020, 8(25): 5500-5514.
47.	Campiglio CE, Villonio M, Dellacà RL, et al. An injectable, degradable hydrogel plug for tracheal occlusion in congenital diaphragmatic hernia (CDH). Mater Sci Eng C Mater Biol Appl, 2019, 99: 430-439.
48.	Perrone EE, Deprest JA. Fetal endoscopic tracheal occlusion for congenital diaphragmatic hernia: A narrative review of the history, current practice, and future directions. Transl Pediatr, 2021, 10(5): 1448-1460.
49.	Campiglio CE, Villonio M, Dellacà RL, et al. An injectable, degradable hydrogel plug for tracheal occlusion in congenital diaphragmatic hernia (CDH). Mater Sci Eng C Mater Biol Appl, 2019, 99: 430-439.

1. Choudhury D, Tun HW, Wang T, et al. Organ-derived decellularized extracellular matrix: A game changer for bioink manufacturing? Trends Biotechnol, 2018 Aug;36(8): 787-805.
2. Rock JR, Randell SH, Hogan BL. Airway basal stem cells: A perspective on their roles in epithelial homeostasis and remodeling. Dis Model Mech, 2010, 3(9-10): 545-556.
3. Li N, Guo R, Zhang ZJ. Bioink formulations for bone tissue regeneration. Front Bioeng Biotechnol, 2021, 9: 630488.
4. Zhang YS, Yue K, Aleman J, et al. 3D Bioprinting for tissue and organ fabrication. Ann Biomed Eng, 2017, 45(1): 148-163.
5. Jungst T, Smolan W, Schacht K, et al. Strategies and molecular design criteria for 3D printable hydrogels. Chem Rev, 2016, 116(3): 1496-539.
6. Garcia-Cruz MR, Postma A, Frith JE, et al. Printability and bio-functionality of a shear thinning methacrylated xanthan-gelatin composite bioink. Biofabrication, 2021, 13(3):doi: 10.1088/1758-5090/abec2d. .
7. Mörö A, Samanta S, Honkamäki L, et al. Hyaluronic acid based next generation bioink for 3D bioprinting of human stem cell derived corneal stromal model with innervation. Biofabrication, 2022, 15(1) :doi: 10.1088/1758-5090/acab34.
8. Shams E, Barzad MS, Mohamadnia S, et al. A review on alginate-based bioinks, combination with other natural biomaterials and characteristics. J Biomater Appl, 2022, 37(2): 355-372.
9. Blaeser A, Duarte Campos DF, Puster U, et al. Controlling shear stress in 3d bioprinting is a key factor to balance printing resolution and stem cell integrity. Adv Healthc Mater, 2016, 5(3): 326-333.
10. Liu W, Heinrich MA, Zhou Y, et al. Extrusion Bioprinting of Shear-Thinning Gelatin Methacryloyl Bioinks. Adv Healthc Mater, 2017, 6(12): 10.1002/adhm. 201601451.
11. Poldervaart MT, Goversen B, de Ruijter M, et al. 3D bioprinting of methacrylated hyaluronic acid (MeHA) hydrogel with intrinsic osteogenicity. PLoS One, 2017, 12(6): e0177628.
12. Gomez-Florit M, Pardo A, Domingues RMA, et al. Natural-based hydrogels for tissue engineering applications. Molecules, 2020, 25(24): 5858.
13. Decante G, Costa JB, Silva-Correia J, et al. Engineering bioinks for 3D bioprinting. Biofabrication, 2021, 13(3).
14. Heinrich MA, Liu W, Jimenez A, et al. 3D Bioprinting: From benches to translational applications. Small, 2019, 15(23): e1805510.
15. Wang Z, Zhang Y, Yin Y, et al. High-strength and injectable supramolecular ion wound hhydrogel self-assembled by monomeric nucleoside for tooth-extractealing. Adv Mater, 2022, 34(13): e2108300.
16. Cha GD, Lee WH, Sunwoo SH, et al. Multifunctional injectable hydrogel for in vivo diagnostic and therapeutic applications. ACS Nano, 2022, 16(1): 554-556.
17. Freeman S, Calabro S, Williams R, et al. Bioink formulation and machine learning-empowered bioprinting optimization. Front Bioeng Biotechnol, 2022,doi: 10.3389/fbioe.2022.913579. .
18. Shin M, Galarraga JH, Kwon MY, et al. Gallol-derived ECM-mimetic adhesive bioinks exhibiting temporal shear-thinning and stabilization behavior. Acta Biomater, 2019, 95: 165-175.
19. Gungor-Ozkerim PS, Inci I, Zhang YS, et al. Bioinks for 3D bioprinting: an overview. Biomater Sci, 2018, 6(5): 915-946.
20. Moeinzadeh S, Park Y, Lin S, et al. In-situ stable injectable collagen-based hydrogels for cell and growth factor delivery. Materialia (Oxf), 2021,doi: 10.1016/j.mtla.2020.100954.
21. Stratesteffen H, Köpf M, Kreimendahl F, et al. GelMA-collagen blends enable drop-on-demand 3D printablility and promote angiogenesis. Biofabrication, 2017, 9(4): 045002.
22. Leucht A, Volz AC, Rogal J, et al. Advanced gelatin-based vascularization bioinks for extrusion-based bioprinting of vascularized bone equivalents. Sci Rep, 2020, 10(1): 5330.
23. McBeth C, Lauer J, Ottersbach M, et al. 3D bioprinting of GelMA scaffolds triggers mineral deposition by primary human osteoblasts. Biofabrication, 2017, 9(1): 015009.
24. Behan K, Dufour A, Garcia O, et al. Methacrylated Cartilage ECM-based hydrogels as injectables and bioinks for cartilage tissue engineering. Biomolecules, 2022, 12(2): 216.
25. Kim BS, Kim H, Gao G, et al. Decellularized extracellular matrix: A step towards the next generation source for bioink manufacturing. Biofabrication, 2017, 9(3): 034104.
26. De Santis MM, Alsafadi HN, Tas S, et al. Extracellular-matrix-reinforced bioinks for 3D bioprinting human tissue. Adv Mater, 2021, 33(3): e2005476.
27. Chimene D, Kaunas R, Gaharwar AK. Hydrogel bioink reinforcement for additive manufacturing: A focused review of emerging strategies. Adv Mater, 2020, 32(1): e1902026.
28. Dubbin K, Tabet A, Heilshorn SC. Quantitative criteria to benchmark new and existing bio-inks for cell compatibility. Biofabrication, 2017, 9(4): 044102.
29. Abdulghani S, Morouço PG. Biofabrication for osteochondral tissue regeneration: Bioink printability requirements. J Mater Sci Mater Med, 2019, 30(2): 20.
30. Matai I, Kaur G, Seyedsalehi A, et al. Progress in 3D bioprinting technology for tissue/organ regenerative engineering. Biomaterials, 2020, 226: 119536.
31. Panda S, Hajra S, Mistewicz K, et al. A focused review on three-dimensional bioprinting technology for artificial organ fabrication. Biomater Sci, 2022, 10(18): 5054-5080.
32. Boscher J, Gachet C, Lanza F, et al. Megakaryocyte culture in 3D methylcellulose-based hydrogel to improve cell maturation and study the impact of stiffness and confinement. J Vis Exp, 2021, (174). doi: 10.3791/62511.
33. Jiang J, Woulfe DS, Papoutsakis ET. Shear enhances thrombopoiesis and formation of microparticles that induce megakaryocytic differentiation of stem cells. Blood, 2014, 124(13): 2094-2103.
34. Duarte Campos DF, Blaeser A, Weber M, et al. Three-dimensional printing of stem cell-laden hydrogels submerged in a hydrophobic high-density fluid. Biofabrication, 2013, 5(1): 015003.
35. Duraj-Thatte AM, Manjula-Basavanna A, Rutledge J, et al. Programmable microbial ink for 3D printing of living materials produced from genetically engineered protein nanofibers. Nat Commun, 2021, 12(1): 6600.
36. Duraj-Thatte AM, Courchesne ND, Praveschotinunt P, et al. Genetically programmable self-regenerating bacterial hydrogels. Adv Mater, 2019, 31(40): e1901826.
37. Yan Z, Yin M, Chen J, et al. Assembly and substrate recognition of curli biogenesis system. Nat Commun, 2020, 11(1): 241.
38. Zandi N, Sani ES, Mostafavi E, et al. Nanoengineered shear-thinning and bioprintable hydrogel as a versatile platform for biomedical applications. Biomaterials, 2021, 267: 120476.
39. Nojoomi A, Tamjid E, Simchi A, et al. Injectable polyethylene glycol-laponite composite hydrogels as articular cartilage scaffolds with superior mechanical and rheological properties. Intern J Polym Mater Polym Biomater, 2017, 66(3): 105-114.
40. Ding X, Gao J, Awada H, et al. Dual physical dynamic bond-based injectable and biodegradable hydrogel for tissue regeneration. J Mater Chem B, 2016, 4(6): 1175-1185.
41. Ren X, Zhou Q, Foulad D, et al. Nanoparticulate mineralized collagen glycosaminoglycan materials directly and indirectly inhibit osteoclastogenesis and osteoclast activation. J Tissue Eng Regen Med, 2019, 13(5): 823-834.
42. Barisón MJ, Nogoceke R, Josino R, et al. Functionalized hydrogels for cartilage repair: The value of secretome-instructive signaling. Int J Mol Sci, 2022, 23(11): 6010.
43. Im S, Choe G, Seok JM, et al. An osteogenic bioink composed of alginate, cellulose nanofibrils, and polydopamine nanoparticles for 3D bioprinting and bone tissue engineering. Int J Biol Macromol, 2022, 205: 520-529.
44. Markstedt K, Mantas A, Tournier I, et al. 3D Bioprinting human chondrocytes with nanocellulose-alginate bioink for cartilage tissue engineering applications. Biomacromolecules, 2015, 16(5): 1489-1496.
45. Freeman S, Calabro S, Williams R, et al. Bioink formulation and machine learning-empowered bioprinting optimization. Front Bioeng Biotechnol, 2022, 10: 913579.
46. Chen Y, Xiong X, Liu X, et al. 3D Bioprinting of shear-thinning hybrid bioinks with excellent bioactivity derived from gellan/alginate and thixotropic magnesium phosphate-based gels. J Mater Chem B, 2020, 8(25): 5500-5514.
47. Campiglio CE, Villonio M, Dellacà RL, et al. An injectable, degradable hydrogel plug for tracheal occlusion in congenital diaphragmatic hernia (CDH). Mater Sci Eng C Mater Biol Appl, 2019, 99: 430-439.
48. Perrone EE, Deprest JA. Fetal endoscopic tracheal occlusion for congenital diaphragmatic hernia: A narrative review of the history, current practice, and future directions. Transl Pediatr, 2021, 10(5): 1448-1460.
49. Campiglio CE, Villonio M, Dellacà RL, et al. An injectable, degradable hydrogel plug for tracheal occlusion in congenital diaphragmatic hernia (CDH). Mater Sci Eng C Mater Biol Appl, 2019, 99: 430-439.

Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Latest ArticlesResearch progress of shear-thinned biological ink in 3D bioprinting tissue trachea

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