Preview

Russian Journal of Transplantology and Artificial Organs

Advanced search

Modern opportunities of regenerative medicine: biofabrication of hollow organs

https://doi.org/10.15825/1995-1191-2019-2-92-103

Abstract

For the treatment of patients with organs damaged or removed by medical indications, transplantation from donors is currently used. High risks of death, lifelong immunosuppression and an acute shortage of donor organs worsen the prospect of their use. Recent advances in the field of biofabrication indicate the imminent possibility of the emergence of real alternatives to the methods currently used. The biomaterials used create a three-dimensional space in which cells can attach, grow and form new tissues with an appropriate structure and function. Modern research pays special attention to the choice of materials and technologies to ensure the mechanical and physiological properties of the newly created tissue. The review examines modem technologies of regenerative medicine, as well as the results of experimental studies in the field of biofabrication for creating scaffolds, tissue-engineering structures, as well as hollow and fragments of complex organs that already have practical implementation.

About the Authors

E. S. Evstratova
National Medical Research Radiological Center of the Ministry of Health of the Russian Federation
Russian Federation

Obninsk



P. V. Shegay
National Medical Research Radiological Center of the Ministry of Health of the Russian Federation; Peoples' Friendship University of Russia of the Ministry of Education and Science of the Russian Federation
Russian Federation

Obninsk; Moscow



S. V. Popov
Peoples' Friendship University of Russia of the Ministry of Education and Science of the Russian Federation
Russian Federation

Popov Sergey Vitalievich

6, Miklukho-Maklaya str., Moscow, 117198, Tel. (910) 477-95-65



N. V. Vorobyev
P.A. Hertsen Moscow Oncology Research Center - branch of the National Medical Research Radiological Center of the Ministry of Health of the Russian Federation
Russian Federation


S. A. Ivanov
A. Tsyb Medical Radiological Research Center - branch of the National Medical Research Radiological Center of the Ministry of Health of the Russian Federation; Peoples' Friendship University of Russia of the Ministry of Education and Science of the Russian Federation
Russian Federation

Obninsk, Moscow



А. D. Kaprin
National Medical Research Radiological Center of the Ministry of Health of the Russian Federation; P.A. Hertsen Moscow Oncology Research Center - branch of the National Medical Research Radiological Center of the Ministry of Health of the Russian Federation; Peoples' Friendship University of Russia of the Ministry of Education and Science of the Russian Federation
Russian Federation

Obninsk



References

1. Got’e SV Homyakov SM. Ocenka pot-rebnosti naseleniya v transplantacii organov, donorskogo resursa i planirovanie effektivnoj seti medicinskih orga-nizacij (centrov transplantacii). Vestnik transplantologii i iskusstvennyh organov. 2013; XV (3): 11-24.

2. Mironov VA. 3D-biopechat’: lyubye organy na zakaz. Iniciativy XXIveka. 2013; 4: 94-100.

3. Gorbatov RO, Romanov AD. Sozdanie organov i tkanej s pomoshch’yu biopechati. Vestnik VolgG-MU. 2017; 3 (63): 3-9.

4. Faris RA, Konkin T, Halpert G. Liver stem cells: a potential source of hepatocytes for the treatment of human liver disease. Artif Organs. 2001; 25: 513-521.

5. Shinoka T, Shum-Tim D, Ma PXet al. Tissue-engineered heart valve leaflets: does cell origin affect outcome? Circulation. 1997; 96: II-102-07.

6. Atala A. Engineering organs. Current Opinion in Biotechnology. 2009; 20: 575-592.

7. Baptista PM, Siddiqui MM, Lozier G et al. The use of whole organ decellularization for the generation of a vascularized liver organoid. Hepatology. 2011; 53: 604-617.

8. Song JJ, Guyette JP, Gilpin SE et al. Regeneration and experimental orthotopic transplantation of a bioengineered kidney. Nat. Med. 2013; 19: 646-651.

9. Hamilton NJ, Kanani M, Roebuck DJ et al. Tissue-engineered tracheal replacement in a child: a 4-year followup study. Am. J. Transplant. 2015; 15 (10): 2750-2757.

10. Maemura T, Shin M, Kinoshita Met al. A tissue-engineered stomach shows presence of proton pump and G-cells in a rat model, resulting in improved anemia following total gastrectomy. Artif. Organs. 2008; 32 (3): 234-239.

11. Sala FG, Kunisaki SM, Ochoa ER et al. Tissue-engineered small intestine and stomach form from autologous tissue in a preclinical large animal model. J. Surg. Res. 2009; 156 (2): 205-212.

12. Bitar KN, Raghavan S. Intestinal tissue engineering: current concepts and future vision of regenerative medicine in the gut. NeurogastroenterolMotil. 2012; 24 (1): 7-9.

13. Bitar KN, Zakhem E. Tissue engineering and regenerative medicine as applied to the gastrointestinal tract. Curr. Opin. Biotechnol. 2013; 24 (5): 909-915.

14. Hendow EK, Guhmann P, Wright B et al. Biomaterials for hollow organ tissue engineering. Fibrogenesis & Tissue Repair. 2016; 9: 3.

15. Bonandrini B, Figliuzzi M, Papadimou E et al. Recel-lularization of well-preserved acellular kidney scaffold using embryonic stem cells. Tissue Eng. Part A. 2014; 20: 1486-1498.

16. Elliott MJ, De Coppi P, Speggiorin S et al. Stem-cell-based, tissue engineered tracheal replacement in a child: a 2-year follow-up study. Lancet. 2012; 380: 994-1000.

17. Basu J, Bertram TA. Regenerative Medicine of the Gastrointestinal Tract. Toxicologic Pathology. 2014; 42: 82-90.

18. Wang A, Tang Z, Park IH et al. Induced pluripotent stem cells for neural tissue engineering. Biomaterials. 2011; 32: 5023-5032.

19. Atala A, Lanza RP. Preface. Methods of Tissue Engineering. San Diego, CA: Academic Press; 2001.

20. Kang H-W, Lee SJ, Ko IK et al. A 3D bioprinting system to produce human-scale tissue constructs with structural integrity. Nature Biotechnology. 2016; 34: 312-319.

21. Chen F, Yoo JJ, Atala A. Acellular collagen matrix as a possible ‘off the shelf’ biomaterial for urethral repair. Urology. 1999; 54 (3): 407-410.

22. Atala A. Engineering tissues, organs and cells. J. Tissue. Eng. Regen. Med. 2007; 1: 83-96.

23. Versteegden LR, van Kampen KA, Janke HP et al. Tubular collagen scaffolds with radial elasticity for hollow organ regeneration. Acta Biomaterialia. 2017; 52: 1-8.

24. Liebert M, Hubbel A, Chung M et al. Expression of mal is associated with urothelial differentiation in vitro: identification by differential display reversetranscripta-se polymerase chain reaction. Differentiation. 1997; 61: 177-185.

25. Atala A. Autologous cell transplantation for urologic reconstruction. J. Urol. 1998; 159: 2-3.

26. Yoo JJ, Meng J, Oberpenning F, Atala A. Bladder augmentation using allogenic bladder submucosa seeded with cells. Urology. 1998; 51: 221-225.

27. Oberpenning F, Meng J, Yoo JJ et al. De novo reconstitution of a functional mammalian urinary bladder by tissue engineering. Nat. Biotechnol. 1999; 17: 149-155.

28. Koh CJ, Atala A. Tissue engineering, stem cells, and cloning: opportunities for regenerative medicine. J. Am. Soc. Nephrol. 2004; 15: 1113-1125.

29. Li ST. Biologic biomaterials: tissue derived biomaterials (collagen). The Biomedical Engineering Handbook. FL: CRS Press; 1995: 627-647.

30. Chattopadhyay S, Raines RT. Review collagen-based biomaterials for wound healing. Biopolymers. 2014; 101: 821-833.

31. Dong C, Lv Y. Application of collagen scaffold in tissue engineering: recent advances and new perspectives. Polymers. 2016; 8: 42.

32. Versteegden LR, Hoogenkamp HR, Lomme RM et al. Design of an elasticized collagen scaffold: a method to induce elasticity in a rigid protein. Acta Biomater. 2016; 15: 277-85.

33. Rowley JA, Madlambayan G, Mooney DJ. Alginate hydrogels as synthetic extracellular matrix materials. Biomaterials. 1999; 20: 45-53.

34. Campbell PG, Weiss LE. Tissue engineering with the aid of inkjet printers. Expert. Opin. Biol. Ther. 2007; 7: 1123-1127.

35. Boland T, Xu T, Damon B et al. Application of inkjet printing to tissue engineering. Biotechnol. J. 2006; 1: 910-917.

36. Xu T, Rohozinski J, Zhao W et al. Inkjet-mediated gene transfection into living cells combined with targeted delivery. Tissue Eng. Part A. 2009; 15: 95-101.

37. Ilkhanizadeh S, Teixeira AI, Hermanson O. Inkjet printing of macromolecules on hydrogels to steer neural stem cell differentiation. Biomaterials. 2007; 28: 39363943.

38. Sadovoj MA, Larionov PM, Samohin AG, Rozhnova OM. Kletochnye matricy dlya celej regene-racii kosti: sovremennoe sostoyanie problemy. 2014; 2: 79-86.

39. Novochadov VV, Semenov PS, Lyabin MP. Innovacionnye podhody k op-timizacii skaffold-tekhnologij na osnove hitozana v tka-nevoj inzhenerii sustavnogo hryashcha. Vestn. Volgogr. gos. un-ta. Ser. 10, Innov. deyat. 2013; 2 (9): 135-143.

40. Novochadov VV. Pro-blema upravleniya kletochnym zaseleniem i remodeliro-vaniem tkaneinzhenernyh matric dlya vosstanovleniya sustavnogo hryashcha (obzor literatury). Vestn. Volgogr. gos. un-ta. Ser. 11, Estestv. nauki. 2013; 1 (5): 19-28.

41. Gilpin A, Yang Y. Decellularization strategies for regenerative medicine: from processing techniques to applications. Biomed. Res. Int. 2017; 983-1534.

42. Maghsoudlou P, Georgiades F, Smith H et al. Optimization of liver decellularization maintains extracellular matrix micro-architecture and composition predisposing to effective cell seeding. PLoS ONE. 2016; 11: e0155324.

43. Maghsoudlou P, Georgiades F, Tyraskis A et al. Preservation of micro-architecture and angiogenic potential in a pulmonary acellular matrix obtained using intermittent intratracheal flow of detergent enzymatic treatment. Biomaterials. 2013; 34: 6638-6648.

44. Chen F, Yoo JJ, Atala A. Acellular collagen matrix as a possible ‘‘off the shelf’’ biomaterial for urethral repair. Urology. 1999; 54: 407-410.

45. Reed AM, Gilding DK. Biodegradable polymers for use in surgery - poly(glycolic)/poly(lactic acid) homo and copolymers: 2. In vitro degradation. Polymer. 1981; 22 (4): 494-498.

46. Eberli D, Filho LF, AtalaA et al. Composite scaffolds for the engineering of hollow organs and tissues. Methods. 2009; 47: 109-115.

47. Bacakova L, Filova E, Rypacek F et al. Cell adhesion on artificial materials for tissue engineering. Physiol. Res. 2004; 53 (Suppl 1): S35-45.

48. le Roux PJ. Endoscopic urethroplasty with unseeded small intestinal submucosa collagen matrix grafts: a pilot study. J. Urol. 2005; 173: 140-143.

49. Fu Q, Deng CL, Liu W et al. Urethral replacement using epidermal cell-seeded tubular acellular bladder collagen matrix. BJUInt. 2007; 99: 1162-1165.

50. Li C, Xu Y, Song L et al. Preliminary experimental study of tissue-engineered urethral reconstruction using oral keratinocytes seeded on BAMG. Urol. Int. 2008; 81: 290-295.

51. Guan Y, Ou L, Hu G et al. Tissue engineering of urethra using human vascular endothelial growth factor gene-modified bladder urothelial cells. Artif Organs. 2008; 32: 91-99.

52. Master VA, Wei G, Liu W et al. Urothlelium facilitates the recruitment and trans-differentiation of fibroblasts into smooth muscle in acellular matrix. J. Urol. 2003; 170: 1628-1632.

53. Leonhauser D, Stollenwerk K, Seifarth V et al. Two differentially structured collagen scaffolds for potential urinary bladder augmentation: proof of concept study in a Gottingen minipig model. J TranslMed. 2017; 15: 3.

54. Hoogenkamp HR, Pot MW, Hafmans TG et al. Scaffolds for whole organ tissue engineering: Construction and in vitro evaluation of a seamless, spherical and hollow collagen bladder construct with appendices. Acta Biomaterial. 2016; 43; 112-121.

55. Atala A, Bauer SB, Soker S et al. Tissue-engineered autologous bladders for patients needing cystoplasty. Lancet. 2006; 367 (9518): 1241-1246.

56. Atala A. Tissue engineering of human bladder. British Medical Bulletin. 2011; 97: 81-104.

57. Rouwkema J, Rivron NC, van Blitterswijk CA. Vascularization in tissue engineering. Trends Biotechnol. 2008; 26: 434-441.

58. Zhao X, Irvine SA, Agrawal A et al. 3D patterned substrates for bioartificial blood vessels - the effect of hydrogels on aligned cells on a biomaterial surface. Acta Biomater. 2015; 26: 159-168.

59. Yao L, Liu J, Andreadis ST. Composite fibrin scaffolds increase mechanical strength and preserve contractility of tissue engineered blood vessels. Pharm. Res.-Dordr. 2008; 25 (5): 1212-1221.

60. Singh RK, Seliktar D, Putnam AJ. Capillary morphogenesis in PEG-collagen hydrogels. Biomaterials. 2013; 34 (37): 9331-9340.

61. Moon JJ, Saik JE, Poche RA. Biomimetic hydrogels with pro-angiogenic properties. Biomaterials. 2010; 31 (14): 3840-3847.

62. Watanabe M, Shin’oka T, Tohyama S et al. Tissue engineered vascular autograft: inferior vena cava replacement in a dog model. Tissue Eng. 2001; 7 (4): 429-439.

63. Ott HC, Matthiesen TS, Goh SK et al. Perfusion-decel-lularized matrix: using nature’s platform to engineer a bioartificial heart. Nat. Med. 2008; 14: 213-221.

64. Wainwright JM, Czajka CA, Patel UB et al. Preparation of cardiac extracellular matrix from an intact porcine heart. Tissue Eng. Part. C. Methods. 2010; 16: 525-532.

65. Oberwallner B, Brodarac A, Choi YH et al. Preparation of cardiac extracellular matrix scaffolds by decellulari-zation of human myocardium. J. Biomed. Mater. Res. A. 2014; 102 (9): 3263-3272.

66. Zimmermann WH, Melnychenko I, Wasmeier G et al. Engineered heart tissue grafts improve systolic and diastolic function in infarcted rat hearts. Nat. Med. 2006; 12: 452-458.

67. Rodrigues MT, Lee SJ, Gomes ME et al. Amniotic fluid-derived stem cells as a cell source for bone tissue engineering. Tissue. Eng. A. 2012; 18: 2518-2527.

68. Williams C, Xie AW, Emani S et al. A comparison of human smooth muscle and mesenchymal stem cells as potential cell sources for tissue-engineered vascular patches. Tissue Eng. A. 2012; 18: 986-998.

69. Ladd MR, Lee SJ, Stitzel JD et al. Co-electrospun dual scaffolding system with potential for muscle-tendon junction tissue engineering. Biomaterials. 2011; 32: 1549-1559.

70. Liu H, Li X, Zhou G et al. Electrospun sulfated silk fibroin nanofibrous scaffolds for vascular tissue engineering. Biomaterials. 2011; 32: 3784-3793.

71. Nakase Y, Nakamura T, Kin S et al. Intra-thoracic esophageal replacement by in situ tissue-engineered esophagus. J. Thorac. Cardiovasc. Surg. 2008; 136: 850-859.

72. Basu J, Mihalko KL, Payne R et al. Extension of bladder based organ regeneration platform for tissue engineering of esophagus. Med. Hypotheses. 2012; 78: 231-234.

73. Basu J, Mihalko KL, Rivera EA et al. Tissue engineering of esophagus and small intestine in rodent injury models. Methods Mol. Biol. 2013; 1001: 311-324.

74. Saxena AK, Kofler K, Ainodhofer H et al. Esophagus tissue engineering: hybrid approach with esophageal epithelium and unidirectional smooth muscle tissue component generation in vitro. J. Gastrointest. Surg. 2009; 13: 1037-1043.

75. Badylak SF, Vorp DA, SpievackAR et al. Esophageal reconstruction with ECM and muscle tissue in a dog model. J. Surg. Res. 2005; 128: 87-97.

76. Tan B, Wei RQ, Tan MY et al. Tissue engineered esophagus by mesenchymal stem cell seeding for esophageal repair in a canine model. J. Surg. Res. 2013; 182 (1): 40-48.

77. Othman R, Morris GE, Shah DA et al. An automated fabrication strategy to create patterned tubular architectures at cell and tissue scales. Biofabrication. 2015; 7 (2): 025003.

78. Speer AL, Sala FG, Matthews JA et al. Murine tissue-engineered stomach demonstrates epithelial differentiation. J. Surg. Res. 2011; 171: 6-14.

79. Nakatsu H, Ueno T, Oga A et al. Influence of mesenchymal stem cells on stomach tissue engineering using small intestinal submucosa. J. Tissue Eng. Regen. Med. 2015; 9: 296-304.

80. Hori Y, Nakamura T, Kimura D et al. Experimental study on tissue engineering of the small intestine by mesenchymal stem cell seeding. J. Surg. Res. 2002; 102: 156-160.

81. Grikscheit TC, Siddique A, Ochoa ER et al. Tissue-engineered small intestine improves recovery after massive small bowel resection. Ann. Surg. 2004; 240: 748-754.

82. Grikscheit TC, Ochoa ER, Ramsanahie A et al. Tissue-engineered large intestine resembles native colon with appropriate in vitro physiology and architecture. Ann. Surg. 2003; 238: 35-41.

83. Sala FG, Matthews JA, Speer AL et al. A multicellular approach forms a significant amount of tissue-engineered small intestine in the mouse. Tissue Eng. A. 2011; 17: 1841-1850.

84. Qin HH, Dunn JC. Small intestinal submucosa seeded with intestinal smooth muscle cells in a rodent jejunal interposition model. J. Surg. Res. 2011; 171: e21-26.

85. Nakase Y, Hagiwara A, Nakamura T et al. Tissue engineering of small intestinal tissue using collagen sponge scaffolds seeded with smooth muscle cells. Tissue Eng. 2006; 12 (2): 403-412.

86. Lee M, Wu BM, Stelzner M et al. Intestinal smooth muscle cell maintenance by basic fibroblast growth factor. Tissue Eng. Part A. 2008; 14 (8): 1395-1402.

87. Bitar KN, Zakhem E. Tissue engineering and regenerative medicine as applied to the gastrointestinal tract. Curr. Opin. Biotechnol. 2013; 24 (5): 909-915.

88. Zakhem E, Raghavan S, Gilmont RR et al. Chitosan-based scaffolds for the support of smooth muscle constructs in intestinal tissue engineering. Biomaterials. 2012; 33: 4810-4817.

89. Raghavan S, Lam MT, Foster LL et al. Bioengineered three-dimensional physiological model of colonic longitudinal smooth muscle in vitro. Tissue Eng. C. Methods. 2010; 16: 999-1009.

90. Vermeulen N, Haddow G, Seymour T et al. 3D bioprint me: a socioethical view of bioprinting human organs and tissues. J. Med. Ethics. 2017; 43: 618-624.

91. Gilbert F, O ’Connell CD, Mladenovska T et al. Print Me an Organ? Ethical and Regulatory Issues Emerging from 3D Bioprinting in Medicine Sci. Eng. Ethics. 2018; 24: 73-91.


Review

For citations:


Evstratova E.S., Shegay P.V., Popov S.V., Vorobyev N.V., Ivanov S.A., Kaprin А.D. Modern opportunities of regenerative medicine: biofabrication of hollow organs. Russian Journal of Transplantology and Artificial Organs. 2019;21(2):92-103. (In Russ.) https://doi.org/10.15825/1995-1191-2019-2-92-103

Views: 1476


Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 License.


ISSN 1995-1191 (Print)