Research advances of three-dimensional bioprinting technology in urinary system tissue engineering_Journal of Biomedical Engineering

Authors：

FU Zhouyang ¹ , XIAO Shuwei ¹ ,  FU Weijun ²

1. Chinese PLA Medical School, Beijing 100853, P. R. China;
2. Department of Urology, the Third Medical Center, Chinese PLA General Hospital, Beijing 100039, P. R. China;

Corresponding?author：

Keywords：

Three-dimensional bioprinting technology; Tissue engineering; Urology; Biomaterials

DOI：

10.7507/1001-5515.202107061

Video：

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For the damage and loss of tissues and organs caused by urinary system diseases, the current clinical treatment methods have limitations. Tissue engineering provides a therapeutic method that can replace or regenerate damaged tissues and organs through the research of cells, biological scaffolds and biologically related molecules. As an emerging manufacturing technology, three-dimensional (3D) bioprinting technology can accurately control the biological materials carrying cells, which further promotes the development of tissue engineering. This article reviews the research progress and application of 3D bioprinting technology in tissue engineering of kidney, ureter, bladder, and urethra. Finally, the main current challenges and future prospects are discussed.

Citation： FU Zhouyang, XIAO Shuwei, FU Weijun. Research advances of three-dimensional bioprinting technology in urinary system tissue engineering. Journal of Biomedical Engineering, 2022, 39(3): 639-644. doi: 10.7507/1001-5515.202107061 Copy

1.	Ishack S, Lipner S R. A review of 3-dimensional skin bioprinting techniques: applications, approaches, and trends. Dermatol Surg, 2020, 46(12): 1500-1505.
2.	Genova T, Roato I, Carossa M, et al. Advances on bone substitutes through 3D bioprinting. Int J Mol Sci, 2020, 21(19): 7012.
3.	Ma Y, Xie L, Yang B, et al. Three-dimensional printing biotechnology for the regeneration of the tooth and tooth-supporting tissues. Biotechnol Bioeng, 2019, 116(2): 452-468.
4.	Cui X, Li J, Hartanto Y, et al. Advances in extrusion 3D bioprinting: a focus on multicomponent hydrogel-based bioinks. Adv Healthc Mater, 2020, 9(15): e1901648.
5.	Li X, Liu B, Pei B, et al. Inkjet bioprinting of biomaterials. Chem Rev, 2020, 120(19): 10793-10833.
6.	Yu C, Schimelman J, Wang P, et al. Photopolymerizable biomaterials and light-based 3D printing strategies for biomedical applications. Chem Rev, 2020, 120(19): 10695-10743.
7.	Yilmaz B, Tahmasebifar A, Baran E T. Bioprinting technologies in tissue engineering. Adv Biochem Eng Biotechnol, 2020, 171: 279-319.
8.	Serex L, Sharma K, Rizov V, et al. Microfluidic-assisted bioprinting of tissues and organoids at high cell concentrations. Biofabrication, 2021, 13(2). DOI: 10.1088/1758-5090/abca80.
9.	Lee A, Hudson A R, Shiwarski D J, et al. 3D bioprinting of collagen to rebuild components of the human heart. Science, 2019, 365(6452): 482-487.
10.	Grigoryan B, Paulsen S J, Corbett D C, et al. Multivascular networks and functional intravascular topologies within biocompatible hydrogels. Science, 2019, 364(6439): 458-464.
11.	Diamantides N, Dugopolski C, Blahut E, et al. High density cell seeding affects the rheology and printability of collagen bioinks. Biofabrication, 2019, 11(4): 045016.
12.	Mohebbi S, Nezhad M N, Zarrintaj P, et al. Chitosan in biomedical engineering: a critical review. Curr Stem Cell Res Ther, 2019, 14(2): 93-116.
13.	Cao N, Song L, Liu W, et al. Prevascularized bladder acellular matrix hydrogel/silk fibroin composite scaffolds promote the regeneration of urethra in a rabbit model. Biomed Mater, 2018, 14(1): 015002.
14.	Xiao S, Wang P, Zhao J, et al. Bi-layer silk fibroin skeleton and bladder acellular matrix hydrogel encapsulating adipose-derived stem cells for bladder reconstruction. Biomater Sci, 2021, 9(18): 6169-6182.
15.	Ali M, Pr A K, Yoo J J, et al. A photo-crosslinkable kidney ECM-derived bioink accelerates renal tissue formation. Adv Healthc Mater, 2019, 8(7): e1800992.
16.	Takasato M, Er P X, Chiu H S, et al. Kidney organoids from human iPS cells contain multiple lineages and model human nephrogenesis. Nature, 2015, 526(7574): 564-568.
17.	Phipson B, Er P X, Combes A N, et al. Evaluation of variability in human kidney organoids. Nat Methods, 2019, 16(1): 79-87.
18.	Homan K A, Kolesky D B, Skylar-Scott M A, et al. Bioprinting of 3D convoluted renal proximal tubules on perfusable chips. Sci Rep, 2016, 6: 34845.
19.	Singh N K, Han W, Nam S A, et al. Three-dimensional cell-printing of advanced renal tubular tissue analogue. Biomaterials, 2020, 232: 119734.
20.	King S M, Higgins J W, Nino C R, et al. 3D proximal tubule tissues recapitulate key aspects of renal physiology to enable nephrotoxicity testing. Front Physiol, 2017, 8: 123.
21.	Homan K A, Gupta N, Kroll K T, et al. Flow-enhanced vascularization and maturation of kidney organoids in vitro. Nat Methods, 2019, 16(3): 255-262.
22.	Lin N Y C, Homan K A, Robinson S S, et al. Renal reabsorption in 3D vascularized proximal tubule models. Proc Natl Acad Sci U S A, 2019, 116(12): 5399-5404.
23.	Lawlor K T, Vanslambrouck J M, Higgins J W, et al. Cellular extrusion bioprinting improves kidney organoid reproducibility and conformation. Nat Mater, 2021, 20(2): 260-271.
24.	Pien N, Palladino S, Copes F, et al. Tubular bioartificial organs: from physiological requirements to fabrication processes and resulting properties. a critical review. Cells Tissues Organs, 2022, 211: 128-154.
25.	Meng L C, Liao W B, Yang S X, et al. Seeding homologous adipose-derived stem cells and bladder smooth muscle cells into bladder submucosa matrix for reconstructing the ureter in a rabbit model. Transplant Proc, 2015, 47(10): 3002-3011.
26.	Janke H P, De Jonge P, Feitz W F J, et al. Reconstruction strategies of the ureter and urinary diversion using tissue engineering approaches. Tissue Eng Part B Rev, 2019, 25(3): 237-248.
27.	De Jonge P, Simaioforidis V, Geutjes P, et al. Ureteral reconstruction with reinforced collagen scaffolds in a porcine model. J Tissue Eng Regen Med, 2018, 12(1): 80-88.
28.	De Jonge P, Sloff M, Janke H P, et al. Ureteral reconstruction in goats using tissue-engineered templates and subcutaneous preimplantation. Tissue Eng Part A, 2018, 24(11-12): 863-872.
29.	Gundogdu G, Okhunov Z, Cristofaro V, et al. Evaluation of bi-layer silk fibroin grafts for tubular ureteroplasty in a porcine defect model. Front Bioeng Biotechnol, 2021, 9: 723559.
30.	Versteegden L R, Van Kampen K A, Janke H P, et al. Tubular collagen scaffolds with radial elasticity for hollow organ regeneration. Acta Biomater, 2017, 52: 1-8.
31.	凌爭云, 趙健, 符偉軍, 等. 膀胱組織工程:膀胱替代治療的新希望. 中華實驗外科雜志, 2021, 38(12): 2534-2537.
32.	Imamura T, Shimamura M, Ogawa T, et al. Biofabricated structures reconstruct functional urinary bladders in radiation-injured rat bladders. Tissue Eng Part A, 2018, 24(21-22): 1574-1587.
33.	Bouhout S, Chabaud S, Bolduc S. Collagen hollow structure for bladder tissue engineering. Mater Sci Eng C Mater Biol Appl, 2019, 102: 228-237.
34.	Pastorek D, Culenova M, Csobonyeiova M, et al. Tissue engineering of the urethra: from bench to bedside. Biomedicines, 2021, 9(12): 1917.
35.	Zhang K, Fu Q, Yoo J, et al. 3D bioprinting of urethra with PCL/PLCL blend and dual autologous cells in fibrin hydrogel: an in vitro evaluation of biomimetic mechanical property and cell growth environment. Acta Biomater, 2017, 50: 154-164.
36.	張楷樂, 楊熙, 牛長梅, 等. 三維生物打印結合海藻酸鈉和纖維蛋白原構建仿生尿道修復補片的實驗研究. 上海醫學, 2019, 42(3): 164-169.
37.	Findrik Balogová A, Hudák R, Tóth T, et al. Determination of geometrical and viscoelastic properties of PLA/PHB samples made by additive manufacturing for urethral substitution. J Biotechnol, 2018, 284: 123-130.
38.	Cunnane E M, Davis N F, Cunnane C V, et al. Mechanical, compositional and morphological characterisation of the human male urethra for the development of a biomimetic tissue engineered urethral scaffold. Biomaterials, 2021, 269: 120651.
39.	Pi Q, Maharjan S, Yan X, et al. Digitally tunable microfluidic bioprinting of multilayered cannular tissues. Adv Mater, 2018, 30(43): e1706913.
40.	Parfenov V A, Koudan E V, Krokhmal A A, et al. Biofabrication of a functional tubular construct from tissue spheroids using magnetoacoustic levitational directed assembly. Adv Healthc Mater, 2020, 9(24): e2000721.
41.	Oh K J, Yu H S, Park J, et al. Co-culture of smooth muscle cells and endothelial cells on three-dimensional bioprinted polycaprolactone scaffolds for cavernosal tissue engineering. Aging Male, 2020, 23(5): 830-835.
42.	Miri A K, Nieto D, Iglesias L, et al. Microfluidics-enabled multimaterial maskless stereolithographic bioprinting. Adv Mater, 2018, 30(27): e1800242.
43.	Yang Q, Gao B, Xu F. Recent advances in 4D bioprinting. Biotechnol J, 2020, 15(1): e1900086.
44.	Ajalloueian F, Lemon G, Hilborn J, et al. Bladder biomechanics and the use of scaffolds for regenerative medicine in the urinary bladder. Nat Rev Urol, 2018, 15(3): 155-174.
45.	Tavafoghi M, Sheikhi A, Tutar R, et al. Engineering tough, injectable, naturally derived, bioadhesive composite hydrogels. Adv Healthc Mater, 2020, 9(10): e1901722.
46.	Zhao F, Zhou L, Xu Z, et al. Hypoxia-preconditioned adipose-derived endothelial progenitor cells promote bladder augmentation. Tissue Eng Part A, 2020, 26(1-2): 78-92.
47.	Kim B S, Gao G, Kim J Y, et al. 3D cell printing of perfusable vascularized human skin equivalent composed of epidermis, dermis, and hypodermis for better structural recapitulation of native skin. Adv Healthc Mater, 2019, 8(7): e1801019.
48.	Ye L, Ji H, Liu J, et al. Carbon nanotube-hydrogel composites facilitate neuronal differentiation while maintaining homeostasis of network activity. Adv Mater, 2021, 33(41): e2102981.
49.	Li X P, Qu K Y, Zhou B, et al. Electrical stimulation of neonatal rat cardiomyocytes using conductive polydopamine-reduced graphene oxide-hybrid hydrogels for constructing cardiac microtissues. Colloids Surf B Biointerfaces, 2021, 205: 111844.
50.	Gillispie G J, Han A, Uzun-Per M, et al. The Influence of printing parameters and cell density on bioink printing outcomes. Tissue Eng Part A, 2020, 26(23-24): 1349-1358.

1. Ishack S, Lipner S R. A review of 3-dimensional skin bioprinting techniques: applications, approaches, and trends. Dermatol Surg, 2020, 46(12): 1500-1505.
2. Genova T, Roato I, Carossa M, et al. Advances on bone substitutes through 3D bioprinting. Int J Mol Sci, 2020, 21(19): 7012.
3. Ma Y, Xie L, Yang B, et al. Three-dimensional printing biotechnology for the regeneration of the tooth and tooth-supporting tissues. Biotechnol Bioeng, 2019, 116(2): 452-468.
4. Cui X, Li J, Hartanto Y, et al. Advances in extrusion 3D bioprinting: a focus on multicomponent hydrogel-based bioinks. Adv Healthc Mater, 2020, 9(15): e1901648.
5. Li X, Liu B, Pei B, et al. Inkjet bioprinting of biomaterials. Chem Rev, 2020, 120(19): 10793-10833.
6. Yu C, Schimelman J, Wang P, et al. Photopolymerizable biomaterials and light-based 3D printing strategies for biomedical applications. Chem Rev, 2020, 120(19): 10695-10743.
7. Yilmaz B, Tahmasebifar A, Baran E T. Bioprinting technologies in tissue engineering. Adv Biochem Eng Biotechnol, 2020, 171: 279-319.
8. Serex L, Sharma K, Rizov V, et al. Microfluidic-assisted bioprinting of tissues and organoids at high cell concentrations. Biofabrication, 2021, 13(2). DOI: 10.1088/1758-5090/abca80.
9. Lee A, Hudson A R, Shiwarski D J, et al. 3D bioprinting of collagen to rebuild components of the human heart. Science, 2019, 365(6452): 482-487.
10. Grigoryan B, Paulsen S J, Corbett D C, et al. Multivascular networks and functional intravascular topologies within biocompatible hydrogels. Science, 2019, 364(6439): 458-464.
11. Diamantides N, Dugopolski C, Blahut E, et al. High density cell seeding affects the rheology and printability of collagen bioinks. Biofabrication, 2019, 11(4): 045016.
12. Mohebbi S, Nezhad M N, Zarrintaj P, et al. Chitosan in biomedical engineering: a critical review. Curr Stem Cell Res Ther, 2019, 14(2): 93-116.
13. Cao N, Song L, Liu W, et al. Prevascularized bladder acellular matrix hydrogel/silk fibroin composite scaffolds promote the regeneration of urethra in a rabbit model. Biomed Mater, 2018, 14(1): 015002.
14. Xiao S, Wang P, Zhao J, et al. Bi-layer silk fibroin skeleton and bladder acellular matrix hydrogel encapsulating adipose-derived stem cells for bladder reconstruction. Biomater Sci, 2021, 9(18): 6169-6182.
15. Ali M, Pr A K, Yoo J J, et al. A photo-crosslinkable kidney ECM-derived bioink accelerates renal tissue formation. Adv Healthc Mater, 2019, 8(7): e1800992.
16. Takasato M, Er P X, Chiu H S, et al. Kidney organoids from human iPS cells contain multiple lineages and model human nephrogenesis. Nature, 2015, 526(7574): 564-568.
17. Phipson B, Er P X, Combes A N, et al. Evaluation of variability in human kidney organoids. Nat Methods, 2019, 16(1): 79-87.
18. Homan K A, Kolesky D B, Skylar-Scott M A, et al. Bioprinting of 3D convoluted renal proximal tubules on perfusable chips. Sci Rep, 2016, 6: 34845.
19. Singh N K, Han W, Nam S A, et al. Three-dimensional cell-printing of advanced renal tubular tissue analogue. Biomaterials, 2020, 232: 119734.
20. King S M, Higgins J W, Nino C R, et al. 3D proximal tubule tissues recapitulate key aspects of renal physiology to enable nephrotoxicity testing. Front Physiol, 2017, 8: 123.
21. Homan K A, Gupta N, Kroll K T, et al. Flow-enhanced vascularization and maturation of kidney organoids in vitro. Nat Methods, 2019, 16(3): 255-262.
22. Lin N Y C, Homan K A, Robinson S S, et al. Renal reabsorption in 3D vascularized proximal tubule models. Proc Natl Acad Sci U S A, 2019, 116(12): 5399-5404.
23. Lawlor K T, Vanslambrouck J M, Higgins J W, et al. Cellular extrusion bioprinting improves kidney organoid reproducibility and conformation. Nat Mater, 2021, 20(2): 260-271.
24. Pien N, Palladino S, Copes F, et al. Tubular bioartificial organs: from physiological requirements to fabrication processes and resulting properties. a critical review. Cells Tissues Organs, 2022, 211: 128-154.
25. Meng L C, Liao W B, Yang S X, et al. Seeding homologous adipose-derived stem cells and bladder smooth muscle cells into bladder submucosa matrix for reconstructing the ureter in a rabbit model. Transplant Proc, 2015, 47(10): 3002-3011.
26. Janke H P, De Jonge P, Feitz W F J, et al. Reconstruction strategies of the ureter and urinary diversion using tissue engineering approaches. Tissue Eng Part B Rev, 2019, 25(3): 237-248.
27. De Jonge P, Simaioforidis V, Geutjes P, et al. Ureteral reconstruction with reinforced collagen scaffolds in a porcine model. J Tissue Eng Regen Med, 2018, 12(1): 80-88.
28. De Jonge P, Sloff M, Janke H P, et al. Ureteral reconstruction in goats using tissue-engineered templates and subcutaneous preimplantation. Tissue Eng Part A, 2018, 24(11-12): 863-872.
29. Gundogdu G, Okhunov Z, Cristofaro V, et al. Evaluation of bi-layer silk fibroin grafts for tubular ureteroplasty in a porcine defect model. Front Bioeng Biotechnol, 2021, 9: 723559.
30. Versteegden L R, Van Kampen K A, Janke H P, et al. Tubular collagen scaffolds with radial elasticity for hollow organ regeneration. Acta Biomater, 2017, 52: 1-8.
31. 凌爭云, 趙健, 符偉軍, 等. 膀胱組織工程:膀胱替代治療的新希望. 中華實驗外科雜志, 2021, 38(12): 2534-2537.
32. Imamura T, Shimamura M, Ogawa T, et al. Biofabricated structures reconstruct functional urinary bladders in radiation-injured rat bladders. Tissue Eng Part A, 2018, 24(21-22): 1574-1587.
33. Bouhout S, Chabaud S, Bolduc S. Collagen hollow structure for bladder tissue engineering. Mater Sci Eng C Mater Biol Appl, 2019, 102: 228-237.
34. Pastorek D, Culenova M, Csobonyeiova M, et al. Tissue engineering of the urethra: from bench to bedside. Biomedicines, 2021, 9(12): 1917.
35. Zhang K, Fu Q, Yoo J, et al. 3D bioprinting of urethra with PCL/PLCL blend and dual autologous cells in fibrin hydrogel: an in vitro evaluation of biomimetic mechanical property and cell growth environment. Acta Biomater, 2017, 50: 154-164.
36. 張楷樂, 楊熙, 牛長梅, 等. 三維生物打印結合海藻酸鈉和纖維蛋白原構建仿生尿道修復補片的實驗研究. 上海醫學, 2019, 42(3): 164-169.
37. Findrik Balogová A, Hudák R, Tóth T, et al. Determination of geometrical and viscoelastic properties of PLA/PHB samples made by additive manufacturing for urethral substitution. J Biotechnol, 2018, 284: 123-130.
38. Cunnane E M, Davis N F, Cunnane C V, et al. Mechanical, compositional and morphological characterisation of the human male urethra for the development of a biomimetic tissue engineered urethral scaffold. Biomaterials, 2021, 269: 120651.
39. Pi Q, Maharjan S, Yan X, et al. Digitally tunable microfluidic bioprinting of multilayered cannular tissues. Adv Mater, 2018, 30(43): e1706913.
40. Parfenov V A, Koudan E V, Krokhmal A A, et al. Biofabrication of a functional tubular construct from tissue spheroids using magnetoacoustic levitational directed assembly. Adv Healthc Mater, 2020, 9(24): e2000721.
41. Oh K J, Yu H S, Park J, et al. Co-culture of smooth muscle cells and endothelial cells on three-dimensional bioprinted polycaprolactone scaffolds for cavernosal tissue engineering. Aging Male, 2020, 23(5): 830-835.
42. Miri A K, Nieto D, Iglesias L, et al. Microfluidics-enabled multimaterial maskless stereolithographic bioprinting. Adv Mater, 2018, 30(27): e1800242.
43. Yang Q, Gao B, Xu F. Recent advances in 4D bioprinting. Biotechnol J, 2020, 15(1): e1900086.
44. Ajalloueian F, Lemon G, Hilborn J, et al. Bladder biomechanics and the use of scaffolds for regenerative medicine in the urinary bladder. Nat Rev Urol, 2018, 15(3): 155-174.
45. Tavafoghi M, Sheikhi A, Tutar R, et al. Engineering tough, injectable, naturally derived, bioadhesive composite hydrogels. Adv Healthc Mater, 2020, 9(10): e1901722.
46. Zhao F, Zhou L, Xu Z, et al. Hypoxia-preconditioned adipose-derived endothelial progenitor cells promote bladder augmentation. Tissue Eng Part A, 2020, 26(1-2): 78-92.
47. Kim B S, Gao G, Kim J Y, et al. 3D cell printing of perfusable vascularized human skin equivalent composed of epidermis, dermis, and hypodermis for better structural recapitulation of native skin. Adv Healthc Mater, 2019, 8(7): e1801019.
48. Ye L, Ji H, Liu J, et al. Carbon nanotube-hydrogel composites facilitate neuronal differentiation while maintaining homeostasis of network activity. Adv Mater, 2021, 33(41): e2102981.
49. Li X P, Qu K Y, Zhou B, et al. Electrical stimulation of neonatal rat cardiomyocytes using conductive polydopamine-reduced graphene oxide-hybrid hydrogels for constructing cardiac microtissues. Colloids Surf B Biointerfaces, 2021, 205: 111844.
50. Gillispie G J, Han A, Uzun-Per M, et al. The Influence of printing parameters and cell density on bioink printing outcomes. Tissue Eng Part A, 2020, 26(23-24): 1349-1358.

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