Advance in functional bladder engineering_Journal of Biomedical Engineering

Authors：

ZHANG Xiuzhen , CHEN Qiuzhu , ZHANG Yiqi ,  XIE Huiqi

The Laboratory of Stem Cell and Tissue Engineering, West China Hospital, Sichuan University, Chengdu 610041, P.R.China;

Corresponding author：

Keywords：

bladder tissue engineering; seeding cell; scaffold; growth factor

DOI：

10.7507/1001-5515.201911075

Video：

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Bladder has many important functions as a urine storage and voiding organ. Bladder injury caused by various pathological factors may need bladder reconstruction. Currently the standard procedure for bladder reconstruction is gastrointestinal replacement. However, due to the significant difference in their structure and function, intestinal segment replacement may lead to complications such as hematuria, dysuria, calculi and tumor. With the recent advance in tissue engineering and regenerative medicine, new techniques have emerged for the repair of bladder defects. This paper reviews the recent progress in three aspects of urinary bladder tissue engineering, i.e., seeding cells, scaffolds and growth factors.

Citation： ZHANG Xiuzhen, CHEN Qiuzhu, ZHANG Yiqi, XIE Huiqi. Advance in functional bladder engineering. Journal of Biomedical Engineering, 2020, 37(2): 200-206. doi: 10.7507/1001-5515.201911075 Copy

1.	Stanasel I, Mirzazadeh M, Smith J J, 3 rd. Bladder tissue engineering. Urol Clin North Am, 2010, 37(4): 593-599.
2.	Chua M E, Farhat W A, Ming J M, et al. Review of clinical experience on biomaterials and tissue engineering of urinary bladder. World J Urol, 2019, 12(4): 58-65.
3.	Lam Van Ba O, Aharony S, Loutochin O, et al. Bladder tissue engineering: a literature review. Adv Drug Deliv Rev, 2015, 82-83: 31-37.
4.	Zhou Z, Yan H, Y L, et al. Adipose-derived stem-cell-implanted poly(ϵ-caprolactone)/chitosan scaffold improves bladder regeneration in a rat model. Regen Med, 2018, 13(3): 331-342.
5.	Hipp J A, Hipp J D, Yoo J J, et al. Microarray analysis of bladder smooth muscle from patients with myelomeningocele. BJU Int, 2008, 102(6): 741-746.
6.	Qin D, Long T, Deng J, et al. Urine-derived stem cells for potential use in bladder repair. Stem Cell Res Ther, 2014, 105(5): 134-141.
7.	le Roux P J. Endoscopic urethroplasty with unseeded small intestinal submucosa collagen matrix grafts: a pilot study. J Urol, 2005, 173(1): 140-143.
8.	Coutu D L, Mahfouz W, Loutochin O. Tissue engineering of rat bladder using marrow-derived mesenchymal stem cells and bladder acellular matrix. PLoS One, 2014, 9(12): 18-26.
9.	Wu R, Liu G, Bharadwaj S, et al. Isolation and myogenic differentiation of mesenchymal stem cells for urologic tissue engineering. Methods Mol Biol, 2013, 1001: 65-80.
10.	Sharma A K, Cheng E Y. Growth factor and small molecule influence on urological tissue regeneration utilizing cell seeded scaffolds. Adv Drug Deliv Rev, 2015, 82-83: 86-92.
11.	Smolar J, Horst M, Sulser T, et al. Bladder regeneration through stem cell therapy. Expert Opin Biol Ther, 2018, 18(5): 525-544.
12.	Leite M T, Freitas-Filho L G, Oliveira A S, et al. The use of mesenchymal stem cells in bladder augmentation. Pediatr Surg Int, 2014, 30(4): 361-370.
13.	Serrano-Aroca A, Vera-Donoso C D, Moreno-Manzano V. Bioengineering approaches for bladder regeneration. Int J Mol Sci, 2018, 19(6): 145-152.
14.	Lin H K, Madihally S V, Palmer B, et al. Biomatrices for bladder reconstruction. Adv Drug Deliv Rev, 2015, 82-83: 47-63.
15.	Yang B, Zhang Y, Zhou L, et al. Development of a porcine bladder acellular matrix with well-preserved extracellular bioactive factors for tissue engineering. Tissue Eng Part C Methods, 2010, 16(5): 1201-1211.
16.	Engelhardt E M, Stegberg E, Brown R A, et al. Compressed collagen gel: a novel scaffold for human bladder cells. J Tissue Eng Regen Med, 2010, 4(2): 123-130.
17.	Mudera V, Morgan M, Cheema U, et al. Ultra-rapid engineered collagen constructs tested in an in vivo nursery site. J Tissue Eng Regen Med, 2007, 1(3): 192-198.
18.	Panilaitis B, Altman G H, Chen J, et al. Macrophage responses to silk. Biomaterials, 2003, 24(18): 3079-3085.
19.	Altman G H, Diaz F, Jakuba C, et al. Silk-based biomaterials. Biomaterials, 2003, 24: 401-416.
20.	Mauney J R, Cannon G M, Lovett M L, et al. Evaluation of gel spun silk-based biomaterials in a murine model of bladder augmentation. Biomaterials, 2011, 32(3): 808-818.
21.	Sack B S, Mauney J R, Estrada C R Jr. Silk fibroin scaffolds for urologic tissue engineering. Curr Urol Rep, 2016, 17(2): 16.
22.	Pawelec K M, Best S M, Cameron R E. Collagen: a network for regenerative medicine. J Mater Chem B, 2016, 4(40): 6484-6496.
23.	Yoo J J, Meng J, Oberpenning F, et al. Bladder augmentation using allogenic bladder submucosa seeded with cells. Adult Urol, 1998, 51: 221-225.
24.	Guyette J P, Gilpin S E, Charest J M, et al. Perfusion decellularization of whole organs. Nat Protoc, 2014, 9(6): 1451-1468.
25.	Piechota H J, Dahms S E, Nunes L S, et al. In vitro functional properties of the rat bladder regenerated by the bladder acellular matrix graft. J Urol, 1998, 159(5): 1717-1724.
26.	Brown A L, Brook-Allred T T, Waddell J E, et al. Bladder acellular matrix as a substrate for studying in vitro bladder smooth muscle-urothelial cell interactions. Biomaterials, 2005, 26(5): 529-543.
27.	Geng H Q, Tang D X, Chen F, et al. The bladder submucosa acellular matrix as a cell deliverer in tissue engineering. World J Pediatr, 2006, 2: 57-60.
28.	He S K, Guo J H, Wang Z L, et al. Efficacy and safety of small intestinal submucosa in dural defect repair in a canine model. Mater Sci Eng C Mater Biol Appl, 2017, 73: 267-274.
29.	Martinez A, Blanco M D, Davidenko N, et al. Tailoring chitosan/collagen scaffolds for tissue engineering: Effect of composition and different crosslinking agents on scaffold properties. Carbohydr Polym, 2015, 132: 606-619.
30.	Cao G, Huang Y, Li K, et al. Small intestinal submucosa: superiority, limitations and solutions, and its potential to address bottlenecks in tissue repair. J Mater Chem B, 2019, 7(33): 5038-5055.
31.	Kropp B P, Rippy M K, Badylak S F, et al. Regenerative urinary bladder augmentation using small intestinal submucosa: urodynamic and histopathologic assessment in long-term canine bladder augmentations. J Urol, 1996, 155(6): 2098-2104.
32.	Sutherland R S, Baskin L S, Hayward S U, et al. Regeneration of bladder urothelium, smooth muscle, blood vessels and nerves into an acellular tissue matrix. J Urol, 1996, 156(2S): 571-577.
33.	Badylak S F, Lantz G C, Coffey A, et al. Small intestinal submucosa as a large diameter vascular graft in the dog. J Surg Res, 1989, 47: 74-80.
34.	Vaught J D, Kropp B P, Sawyer B D, et al. Detrusor regeneration in the rat using porcine small intestinal submucosal grafts: functional innervation and receptor expression. J Urol, 1996, 155: 374-378.
35.	Lin H K, Godiwalla S Y, Palmer B, et al. Understanding roles of porcine small intestinal submucosa in urinary bladder regeneration: Identification of variable regenerative characteristics of small intestinal submucosa. Tissue Engineering Part B: Reviews, 2014, 20(1): 73-83.
36.	El-Taji O M, Khattak A Q, Hussain S A. Bladder reconstruction: The past, present and future. Oncol Lett, 2015, 10(1): 3-10.
37.	Baker S C, Atkin N, Gunning P A, et al. Characterisation of electrospun polystyrene scaffolds for three-dimensional in vitro biological studies. Biomaterials, 2006, 27(16): 3136-3146.
38.	Rohman G, Pettit J J, Isaure F, et al. Influence of the physical properties of two-dimensional polyester substrates on the growth of normal human urothelial and urinary smooth muscle cells in vitro. Biomaterials, 2007, 28(14): 2264-2274.
39.	Ardeshirylajimi A, Ghaderian S M, Omrani M D, et al. Biomimetic scaffold containing PVDF nanofibers with sustained TGF-beta release in combination with AT-MSCs for bladder tissue engineering. Gene, 2018, 676: 195-201.
40.	Engelhardt E M, Micol L A, Houis S, et al. A collagen-poly (lactic acid-co-ɛ-caprolactone) hybrid scaffold for bladder tissue regeneration. Biomaterials, 2011, 32(16): 3969-3976.
41.	Xiao D, Yan H, Wang Q, et al. Trilayer three-dimensional hydrogel composite scaffold containing encapsulated adipose-derived stem cells promotes bladder reconstruction via SDF-1alpha/CXCR4 pathway. ACS Appl Mater Interfaces, 2017, 9(44): 38230-38241.
42.	Toosi K K, Nagatomi J, Chancellor M B, et al. The effects of long-term spinal cord injury on mechanical properties of the rat urinary bladder. Ann Biomed Eng, 2008, 36(9): 1470-1480.
43.	Guilak F, Butler D L, Goldstein S A, et al. Biomechanics and mechanobiology in functional tissue engineering. J Biomech, 2014, 47(9): 1933-1940.
44.	Hastings C L, Roche E T, Ruiz-Hernandez E, et al. Drug and cell delivery for cardiac regeneration. Adv Drug Deliv Rev, 2015, 84: 85-106.
45.	Smolar J, Salemi S, Horst M, et al. Stem cells in functional bladder engineering. Transfus Med Hemother, 2016, 43(5): 328-335.
46.	Zhang D, Cao N, Zhou S, et al. The enhanced angiogenesis effect of VEGF-silk fibroin nanospheres-BAMG scaffold composited with adipose derived stem cells in a rabbit model. RSC Advances, 2018, 8(27): 15158-15165.
47.	Youssif M, Shiina H, Urakami S, et al. Effect of vascular endothelial growth factor on regeneration of bladder acellular matrix graft: histologic and functional evaluation. Urology, 2005, 66(1): 201-207.
48.	Jiang X, Lin H, Jiang D, et al. Co-delivery of VEGF and bFGF via a PLGA nanoparticle-modified BAM for effective contracture inhibition of regenerated bladder tissue in rabbits. Sci Rep, 2016, 6(1): 136-144.
49.	Kanematsu A, Yamamoto S, Noguchi T, et al. Bladder regeneration by bladder acellular matrix combined with sustained release of exogenous growth factor. J Urol, 2003, 170(4 Pt 2): 1633-1638.
50.	Shi C, Chen W, Chen B, et al. Bladder regeneration in a canine model using a bladder acellular matrix loaded with a collagen-binding bFGF. Biomater Sci, 2017, 5(12): 2427-2436.
51.	Jia G, Mitra A K, Gangahar D M, et al. Insulin-like growth factor-1 induces phosphorylation of PI3K-Akt/PKB to potentiate proliferation of smooth muscle cells in human saphenous vein. Exp Mol Pathol, 2010, 89(1): 20-26.
52.	Allen T R, Krueger K D, Hunter W J, et al. Evidence that insulin-like growth factor-1 requires protein kinase C-ɛ, PI3-kinase and mitogen-activated protein kinase pathways to protect human vascular smooth muscle cells from apoptosis. Immunol Cell Biol, 2005, 83(6): 651-667.
53.	Lorentz K M, Yang L, Frey P, et al. Engineered insulin-like growth factor-1 for improved smooth muscle regeneration. Biomaterials, 2012, 33(2): 494-503.
54.	Vardar E, Larsson H M, Engelhardt E M, et al. IGF-1-containing multi-layered collagen-fibrin hybrid scaffolds for bladder tissue engineering. Acta Biomater, 2016, 41: 75-85.

1. Stanasel I, Mirzazadeh M, Smith J J, 3 rd. Bladder tissue engineering. Urol Clin North Am, 2010, 37(4): 593-599.
2. Chua M E, Farhat W A, Ming J M, et al. Review of clinical experience on biomaterials and tissue engineering of urinary bladder. World J Urol, 2019, 12(4): 58-65.
3. Lam Van Ba O, Aharony S, Loutochin O, et al. Bladder tissue engineering: a literature review. Adv Drug Deliv Rev, 2015, 82-83: 31-37.
4. Zhou Z, Yan H, Y L, et al. Adipose-derived stem-cell-implanted poly(ϵ-caprolactone)/chitosan scaffold improves bladder regeneration in a rat model. Regen Med, 2018, 13(3): 331-342.
5. Hipp J A, Hipp J D, Yoo J J, et al. Microarray analysis of bladder smooth muscle from patients with myelomeningocele. BJU Int, 2008, 102(6): 741-746.
6. Qin D, Long T, Deng J, et al. Urine-derived stem cells for potential use in bladder repair. Stem Cell Res Ther, 2014, 105(5): 134-141.
7. le Roux P J. Endoscopic urethroplasty with unseeded small intestinal submucosa collagen matrix grafts: a pilot study. J Urol, 2005, 173(1): 140-143.
8. Coutu D L, Mahfouz W, Loutochin O. Tissue engineering of rat bladder using marrow-derived mesenchymal stem cells and bladder acellular matrix. PLoS One, 2014, 9(12): 18-26.
9. Wu R, Liu G, Bharadwaj S, et al. Isolation and myogenic differentiation of mesenchymal stem cells for urologic tissue engineering. Methods Mol Biol, 2013, 1001: 65-80.
10. Sharma A K, Cheng E Y. Growth factor and small molecule influence on urological tissue regeneration utilizing cell seeded scaffolds. Adv Drug Deliv Rev, 2015, 82-83: 86-92.
11. Smolar J, Horst M, Sulser T, et al. Bladder regeneration through stem cell therapy. Expert Opin Biol Ther, 2018, 18(5): 525-544.
12. Leite M T, Freitas-Filho L G, Oliveira A S, et al. The use of mesenchymal stem cells in bladder augmentation. Pediatr Surg Int, 2014, 30(4): 361-370.
13. Serrano-Aroca A, Vera-Donoso C D, Moreno-Manzano V. Bioengineering approaches for bladder regeneration. Int J Mol Sci, 2018, 19(6): 145-152.
14. Lin H K, Madihally S V, Palmer B, et al. Biomatrices for bladder reconstruction. Adv Drug Deliv Rev, 2015, 82-83: 47-63.
15. Yang B, Zhang Y, Zhou L, et al. Development of a porcine bladder acellular matrix with well-preserved extracellular bioactive factors for tissue engineering. Tissue Eng Part C Methods, 2010, 16(5): 1201-1211.
16. Engelhardt E M, Stegberg E, Brown R A, et al. Compressed collagen gel: a novel scaffold for human bladder cells. J Tissue Eng Regen Med, 2010, 4(2): 123-130.
17. Mudera V, Morgan M, Cheema U, et al. Ultra-rapid engineered collagen constructs tested in an in vivo nursery site. J Tissue Eng Regen Med, 2007, 1(3): 192-198.
18. Panilaitis B, Altman G H, Chen J, et al. Macrophage responses to silk. Biomaterials, 2003, 24(18): 3079-3085.
19. Altman G H, Diaz F, Jakuba C, et al. Silk-based biomaterials. Biomaterials, 2003, 24: 401-416.
20. Mauney J R, Cannon G M, Lovett M L, et al. Evaluation of gel spun silk-based biomaterials in a murine model of bladder augmentation. Biomaterials, 2011, 32(3): 808-818.
21. Sack B S, Mauney J R, Estrada C R Jr. Silk fibroin scaffolds for urologic tissue engineering. Curr Urol Rep, 2016, 17(2): 16.
22. Pawelec K M, Best S M, Cameron R E. Collagen: a network for regenerative medicine. J Mater Chem B, 2016, 4(40): 6484-6496.
23. Yoo J J, Meng J, Oberpenning F, et al. Bladder augmentation using allogenic bladder submucosa seeded with cells. Adult Urol, 1998, 51: 221-225.
24. Guyette J P, Gilpin S E, Charest J M, et al. Perfusion decellularization of whole organs. Nat Protoc, 2014, 9(6): 1451-1468.
25. Piechota H J, Dahms S E, Nunes L S, et al. In vitro functional properties of the rat bladder regenerated by the bladder acellular matrix graft. J Urol, 1998, 159(5): 1717-1724.
26. Brown A L, Brook-Allred T T, Waddell J E, et al. Bladder acellular matrix as a substrate for studying in vitro bladder smooth muscle-urothelial cell interactions. Biomaterials, 2005, 26(5): 529-543.
27. Geng H Q, Tang D X, Chen F, et al. The bladder submucosa acellular matrix as a cell deliverer in tissue engineering. World J Pediatr, 2006, 2: 57-60.
28. He S K, Guo J H, Wang Z L, et al. Efficacy and safety of small intestinal submucosa in dural defect repair in a canine model. Mater Sci Eng C Mater Biol Appl, 2017, 73: 267-274.
29. Martinez A, Blanco M D, Davidenko N, et al. Tailoring chitosan/collagen scaffolds for tissue engineering: Effect of composition and different crosslinking agents on scaffold properties. Carbohydr Polym, 2015, 132: 606-619.
30. Cao G, Huang Y, Li K, et al. Small intestinal submucosa: superiority, limitations and solutions, and its potential to address bottlenecks in tissue repair. J Mater Chem B, 2019, 7(33): 5038-5055.
31. Kropp B P, Rippy M K, Badylak S F, et al. Regenerative urinary bladder augmentation using small intestinal submucosa: urodynamic and histopathologic assessment in long-term canine bladder augmentations. J Urol, 1996, 155(6): 2098-2104.
32. Sutherland R S, Baskin L S, Hayward S U, et al. Regeneration of bladder urothelium, smooth muscle, blood vessels and nerves into an acellular tissue matrix. J Urol, 1996, 156(2S): 571-577.
33. Badylak S F, Lantz G C, Coffey A, et al. Small intestinal submucosa as a large diameter vascular graft in the dog. J Surg Res, 1989, 47: 74-80.
34. Vaught J D, Kropp B P, Sawyer B D, et al. Detrusor regeneration in the rat using porcine small intestinal submucosal grafts: functional innervation and receptor expression. J Urol, 1996, 155: 374-378.
35. Lin H K, Godiwalla S Y, Palmer B, et al. Understanding roles of porcine small intestinal submucosa in urinary bladder regeneration: Identification of variable regenerative characteristics of small intestinal submucosa. Tissue Engineering Part B: Reviews, 2014, 20(1): 73-83.
36. El-Taji O M, Khattak A Q, Hussain S A. Bladder reconstruction: The past, present and future. Oncol Lett, 2015, 10(1): 3-10.
37. Baker S C, Atkin N, Gunning P A, et al. Characterisation of electrospun polystyrene scaffolds for three-dimensional in vitro biological studies. Biomaterials, 2006, 27(16): 3136-3146.
38. Rohman G, Pettit J J, Isaure F, et al. Influence of the physical properties of two-dimensional polyester substrates on the growth of normal human urothelial and urinary smooth muscle cells in vitro. Biomaterials, 2007, 28(14): 2264-2274.
39. Ardeshirylajimi A, Ghaderian S M, Omrani M D, et al. Biomimetic scaffold containing PVDF nanofibers with sustained TGF-beta release in combination with AT-MSCs for bladder tissue engineering. Gene, 2018, 676: 195-201.
40. Engelhardt E M, Micol L A, Houis S, et al. A collagen-poly (lactic acid-co-ɛ-caprolactone) hybrid scaffold for bladder tissue regeneration. Biomaterials, 2011, 32(16): 3969-3976.
41. Xiao D, Yan H, Wang Q, et al. Trilayer three-dimensional hydrogel composite scaffold containing encapsulated adipose-derived stem cells promotes bladder reconstruction via SDF-1alpha/CXCR4 pathway. ACS Appl Mater Interfaces, 2017, 9(44): 38230-38241.
42. Toosi K K, Nagatomi J, Chancellor M B, et al. The effects of long-term spinal cord injury on mechanical properties of the rat urinary bladder. Ann Biomed Eng, 2008, 36(9): 1470-1480.
43. Guilak F, Butler D L, Goldstein S A, et al. Biomechanics and mechanobiology in functional tissue engineering. J Biomech, 2014, 47(9): 1933-1940.
44. Hastings C L, Roche E T, Ruiz-Hernandez E, et al. Drug and cell delivery for cardiac regeneration. Adv Drug Deliv Rev, 2015, 84: 85-106.
45. Smolar J, Salemi S, Horst M, et al. Stem cells in functional bladder engineering. Transfus Med Hemother, 2016, 43(5): 328-335.
46. Zhang D, Cao N, Zhou S, et al. The enhanced angiogenesis effect of VEGF-silk fibroin nanospheres-BAMG scaffold composited with adipose derived stem cells in a rabbit model. RSC Advances, 2018, 8(27): 15158-15165.
47. Youssif M, Shiina H, Urakami S, et al. Effect of vascular endothelial growth factor on regeneration of bladder acellular matrix graft: histologic and functional evaluation. Urology, 2005, 66(1): 201-207.
48. Jiang X, Lin H, Jiang D, et al. Co-delivery of VEGF and bFGF via a PLGA nanoparticle-modified BAM for effective contracture inhibition of regenerated bladder tissue in rabbits. Sci Rep, 2016, 6(1): 136-144.
49. Kanematsu A, Yamamoto S, Noguchi T, et al. Bladder regeneration by bladder acellular matrix combined with sustained release of exogenous growth factor. J Urol, 2003, 170(4 Pt 2): 1633-1638.
50. Shi C, Chen W, Chen B, et al. Bladder regeneration in a canine model using a bladder acellular matrix loaded with a collagen-binding bFGF. Biomater Sci, 2017, 5(12): 2427-2436.
51. Jia G, Mitra A K, Gangahar D M, et al. Insulin-like growth factor-1 induces phosphorylation of PI3K-Akt/PKB to potentiate proliferation of smooth muscle cells in human saphenous vein. Exp Mol Pathol, 2010, 89(1): 20-26.
52. Allen T R, Krueger K D, Hunter W J, et al. Evidence that insulin-like growth factor-1 requires protein kinase C-ɛ, PI3-kinase and mitogen-activated protein kinase pathways to protect human vascular smooth muscle cells from apoptosis. Immunol Cell Biol, 2005, 83(6): 651-667.
53. Lorentz K M, Yang L, Frey P, et al. Engineered insulin-like growth factor-1 for improved smooth muscle regeneration. Biomaterials, 2012, 33(2): 494-503.
54. Vardar E, Larsson H M, Engelhardt E M, et al. IGF-1-containing multi-layered collagen-fibrin hybrid scaffolds for bladder tissue engineering. Acta Biomater, 2016, 41: 75-85.

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