Esophageal organoids: possibility of creating and potential implications for tissue engineering

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Abstract

Esophageal cancer, congenital anomalies, traumatic injuries and prolonged deformities of the esophagus often require radical surgical treatment followed by multi-stage organ reconstruction. Such operations are traumatic for the patient, and the use of the donor esophagus is associated with the need for prolonged immunosuppression. To replace a damaged tissue of the esophagus tissue-engineering structures can be applied. These tissue-engineering structures are based on the use of the association of differentiated or stem cells and natural or synthetic scaffolds, to create an artificial organ in vitro that can mimic an organ. Such formulations can be successfully used to study the development of organs, pathogenesis of diseases and preclinical studies of drugs as so-called "organoids”, and may also have a prospect for clinical use as tissue-engineered prototypes of the esophagus. This review describes the possibilities of using esophageal organoids, systematizes the literature data on studies on the creation of organoids and tissue-engineered prototypes and their effect on the experimental model in transplantation.

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About the authors

Z. E Gilazieva

Kazan (Volga region) Federal University

Email: gilazievazarema@mail.ru

S. S Arkhipova

Kazan (Volga region) Federal University

M. N Zhuravleva

Kazan (Volga region) Federal University

References

  1. Zhang Y. Epidemiology of esophageal cancer. World J. Gastroenterol. 2013; 19(34): 5598-606.
  2. Каприн А.Д., Старинский В.В., редакторы. Злокачественные новообразования в России в 2016 году (заболеваемость и смертность). Россия: МНИОИ им. П.А. Герцена филиал ФГБУ «НМИЦ радиологии» Минздрава России; 2018.
  3. Tröbs R.B., Finke W., Bahr M. et al. Isolated tracheoesophageal fistula versus esophageal atresia - Early morbidity and short-term out-come. A single institution series. Int. J. Pediatr. Otorhinolaryngol. 2017; 94: 104-11.
  4. Буеверов А.О., Лапина Т.Л., Охлобыстин А.В. Ахалазия кардии. В: Ивашкин В.Т., редактор. Гастроэнтерология: Клинические рекомендации. 2-изд. Россия: ГЭОТАР-Медиа; 2009. С. 1-12.
  5. Ивашкин В.Т., Маев И.В., Трухманов А.С. и др. Клинические рекомендации Российской гастроэнтерологической ассоциации по диагностике и лечению гастроэзофагеальной рефлюксной болезни. Рос. Журн. гастроэнтерол. гепатол. колопроктол. 2017; 27(4): 75-95.
  6. Сторонова О., Джахая Н., Трухманов А. Роль защитных факторов слизистой оболочки пищевода в лечении гастроэзофагеальной рефлюксной болезни. Клин. перспективы гастроэнтерологии, гепатологии 2014; 5: 37-42.
  7. Khan M., Santana J., Donnellan С. et al. Medical treatments in the short-term management of reflux oesophagitis. Cochrane Database Syst Rev. 2007; 2: CD003244.
  8. Van Boeckel P., Siersema P.D. Refractory esophageal strictures: what to do when dilation fails. Current Treatment Options in Gastroenterology 2015; 13(1): 47-58.
  9. Harlak A., Yigit T., Coskun K. et.al. Surgical treatment of caustic esophageal strictures in adults. Int. J. Surg. 2013; 11(2): 164-8.
  10. Gossot D., Lefebvre J.F. Ischaemic atrophy of the cervical portion of a substernal colic transplant: successful reconstruction using a synthetic resorbable tube. Br. J. Surg. 1988; 75: 801-2.
  11. Freud E., Efrati I., Kidron D. et al. Comparative experimental study of esophageal wall regeneration after prosthetic replacement. Biomed. Mater. Res. 1999; 45(2): 84-91.
  12. Macchiarini P., Mazmanian G.M., de Montpréville V. et al. Experimental tracheal and tracheoesophageal allotransplantation. Paris-Sud University Lung Transplantation Group. Thorac. Cardiovasc. Surg. 1995; 110: 1037-46.
  13. Freud E., Efrati I., Kidron D. et al. Comparative experimental study of esophageal wall regeneration after prosthetic replacement. Biomed. Mater. Res. 1999; 45(2): 84-91.
  14. Hirdes M.M., Vleggaar F.P., Siersema P.D. Stent placement for esophageal strictures: an update. Expert Rev. Med. Devices 2011; 8(6): 733-55.
  15. Saxena A.K. Esophagus tissue engineering: designing and crafting the components for the "hybrid construct” approach. Eur. J. Pediatr. Surg. 2014; 24(3): 246-62.
  16. Nadkarni R.R., Abed S., Draper J.S. Organoids as a model system for studying human lung development and disease. Biochem. Biophys. Res. Commun. 2016; 473(3): 675-82.
  17. Hynds R.E., Giangreco A. Concise review: the relevance of human stem cell-derived organoid models for epithelial translational medicine. Stem Cells 2013; 31(3): 417-22.
  18. Fang Y., Eglen R.M. Three-Dimensional Cell Cultures in Drug Discovery and Development. S_AS Discovery 2017; 22(5): 456-72.
  19. Dedhia P.H., Bertaux-Skeirik N., Zavros Y. et al. Organoid Models of Human Gastrointestinal Development and Disease. Gastroenterology 2016; 150: 1098-112.
  20. Chanson _., Brownfield D., Garbe J.C. et al. Self-organization is a dynamic and lineage-intrinsic property of mammary epithelial cells. Proceedings of the National Academy of Sciences of the United States of America 2011; 108(8): 3264-9.
  21. Tait I.S., Flint N., Campbell F.C. et al. Generation of neomucosa in vivo by transplantation of dissociated rat postnatal small intestinal epithelium. Differentiation 1994; 56: 91-100.
  22. DeWard A.D., Cramer J., Lagasse E. Cellular heterogeneity in the mouse esophagus implicates the presence of a nonquiescent epithelial stem cell population. Cell Rep. 2014; 9(2): 701-11.
  23. Sato T., Vries R.G., Snippert H.J. et al. Single _gr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 2009; 459: 262-5.
  24. Ootani A., _i X., Sangiorgi E. Sustained in vitro intestinal epithelial culture within a Wnt-dependent stem cell niche. Nat. Med. 2009; 15: 701-6.
  25. Doupe D.P. A single progenitor population switches behavior to maintain and repair esophageal epithelium. Science 2012; 337: 1091-3.
  26. Giroux V., Lento A.A., Islam M. et al. Long-lived keratin 15+ esophageal progenitor cells contribute to homeostasis and regeneration. J. Clin. Invest. 2017; 127(6): 2378-91.
  27. Whelan K. Esophageal 3D culture systems as modeling tools in esophageal epithelial pathobiology and personalized medicine. Cellular and Molecular Gastroenterology and Hepatology 2018; 5: 461-78.
  28. Kasagi Y., Chandramouleeswaran P.M., Whelan K.A. et al. The esophageal organoid system reveals functional interplay between Notch and cytokines in reactive epithelial changes. Cell. Mol. Gastroenterol. Hepatol. 2018; 5: 333-52.
  29. Дергилев К.В., Макаревич П.И., Меньшиков М.Ю. и др. Применение тканеинженерных конструкций на основе пластов клеток для восстановления тканей и органов. Гены и клетки 2016; 11(3): 23-32.
  30. Ameen A., Xingnan L., Cantrell M. et al. Gastrointestinal organoid cultures for functional evaluation of oncogenic loci. Journal of Clinical Oncology 2015; 33: 85-95.
  31. Spurrier R.G., Speer A.L., Hou X. et al. Murine and human tissue-engineered esophagus form from sufficient stem/progenitor cells and do not require microdesigned biomaterials. Tissue Eng. Part A 2015; 21: 906-15.
  32. Streuli C.H., Bailey N., Bissell M.J. Control of mammary epithelial differentiation: basement membrane induces tissue-specific gene expression in the absence of cell-cell interaction and morphological polarity. Cell Biol. 1991; 115: 1383-95.
  33. Miki H., Ando N., Ozawa S. et al. An artificial esophagus constructed of cultured humanesophageal epithelial cells, fibroblasts, polyglycolic acid mesh, and collagen. ASAIO 1999; 45: 502-8.
  34. Kalabis J., Wong G.S., Vega M.E. et al. Isolation and characterization of mouse and human esophageal epithelial cells in 3 organotypic culture. Nat. Protoc. 2012; 7(2): 235-46.
  35. Vrana N.E., Lavalle P., Dokmeci M.R. et al. Engineering functional epithelium for regenerative medicine and in vitro organ models: a review. Tissue Engineering Part B: Reviews 2013; 19(6): 529-43.
  36. Nakase Y., Nakamura T., Kin S. et al. Intrathoracic esophageal replacement by in situ tissue-engineered esophagus. J. Thorac. Cardiovasc. Surg. 2008; 136: 850-9.
  37. Jensen T., Blanchette A., Vadasz S. et al. Biomimetic and synthetic esophageal tissue engineering. Biomaterials 2015; 57: 133-41.
  38. Jungebluth P., Bader A., Baiguera S. et al. The concept of in vivo airway tissue engineering. Biomaterials 2012; 33(17): 4319-26.
  39. Kim B.S., Mooney D.J. Scaffolds for engineering smooth muscle under cyclic mechanical strain conditions. Biomech. Eng. 2000; 122(3): 210-5.
  40. Dhandayuthapani B., Krishnan U.M., Sethuraman S. Fabrication and characterization of chitosan-gelatin blend nanofibers for skin tissue engineering. Biomed. Mater. Res. Part B: Appl. Biomater. 2010; 94(1): 264-72.
  41. Saxena A.K., Ainoedhofer H., Höllwarth M.E. Esophagus tissue engineering: in vitro generation of esophageal epithelial cell sheets and viability on scaffold. Pediatr. Surg. 2009; 44: 896-901.
  42. Saxena A.K., Ainoedhofer H., Höllwarth M.E. Culture of ovine esophageal epithelial cells and in vitro esophagus tissue engineering. Tissue Eng. Part C: Methods 2010; 16: 109-14
  43. Bhrany A.D., Beckstead B.L., Lang T.C. et al. Development of an esophagus acellular matrix tissue scaffold. Tissue Eng. 2006; 12: 319-28.
  44. Beckstead B.L., Pan S., Bhrany A.D. et al. Esophageal epithelial cell interaction with synthetic and natural scaffolds for tissue engineering. Bio-materials 2005; 26: 6217-28.
  45. Jungebluth P., Bader A., Baiguera S. et al. The concept of in vivo airway tissue engineering. Biomaterials 2012; 33(17): 4319-26.
  46. Thorrez L., Shansky J., Wang L. Growth, differentiation, transplantation and survival of human skeletal myofibers on biodegradable scaffolds. Biomaterials 2008; 29(1): 75-84.
  47. Mattei G., Magliaro C., Pirone A. et al. Decellularized human liver is too heterogeneous for designing a generic extracellular matrix mimic hepatic scaffold. Artif. Organs 2017; 41(12): 347-55.
  48. Hwang J., San B.H., Turner N.J. et al. Molecular assessment of collagen denaturation in decellularized tissues using a collagen hybridizing peptide. Acta Biomater. 2017; 53: 268-78.
  49. Hynds R.E., Giangreco A. Concise review: the relevance of human stem cell-derived organoid models for epithelial translational medicine. Stem Cells 2013; 31(3): 417-22.
  50. Velasco M.A., Narvaez-Tovar C.A., Garzôn-Alvarado D.A. Design, materials, and mechanobiology of diodegradable scaffolds for bone tissue engineering. Biomed Res Int. 2015; 2015: 729076.
  51. Makadia H.K., Siegel S.J. Poly Lactic-co-Glycolic acid (PLGA) as biodegradable controlled drug delivery carrier. Polymers 2011; 3(3): 1377-97.
  52. Al-Ahmad A., Schubert C., Carvalho C. et al. Comparison of bacterial adhesion andcellular proliferation on newly developed three-dimensional scaffolds manufactured by rapid prototyping technology. Biomed. Mater. Res. Part A 2011; 98(2): 303-11.
  53. Kuppan P., Sethuraman S., Krishnan M. Poly(3-hydroxybutyrate-co-3-hydroxyvalerate)-based nanofibrous scaffolds to support functional esophageal epithelial cells towards engineering the esophagus. Journal of Biomaterials Science, Polymer Edition 2014; 25(6): 574-93.
  54. Srikanth P., editor. Handbook of bioplastics and biocomposites engineering applications. USA: John Wiley & Sons; 2011.
  55. Hou L., Jin J., Lv J. et al. Constitution and in vivo test of micro-porous tubular scaffold for esophageal tissue engineering. Biomater. Appl. 2015; 30(5): 568-78.
  56. Chen F.M, Liu X. Advancing biomaterials of human origin for tissue engineering. Prog. Polym. Sci. 2016; 53: 86-168.
  57. Fan M.R., Gong M., Da L.C. et al. Tissue engineered esophagus scaffold constructed with porcine small intestinal submucosa and synthetic polymers, https://www.ncbi.nlm.nih.gov/pubmed/24457267.
  58. Patel M., Fisher J.P. Biomaterial scaffolds in pediatric tissue engineering. Pediatr. Res. 2008; 63(5): 497-501.
  59. Burkersroda F., Schedl _., Göpferich A. Why degradable polymers undergo surface erosion or bulk erosion. Biomaterials 2002; 23(21): 4221-31.
  60. Lynen J.P., Klinge U., Anurov M. et al. Surgical mesh as a scaffold for tissue regeneration in the esophagus. Eur. Surg. Res. 2004; 36: 104-11.
  61. Zhuravleva M., Gilazieva Z., Grigoriev T.E. In vitro assessment of electrospun polyamide-6 scaffolds for esophageal tissue engineering. J Biomed Mater Res B Appl Biomater. 2018, [Epub ahead of print].
  62. Hajicharalambous C.S., Lichter J., Hix W.T. et al. Nano- and sub-micron porous polyelectrolyte multilayer assemblies: biomimetic surfaces for human corneal epithelial cells. Biomaterials 2009; 30: 4029-36.
  63. Yoon H., Kim G. Micro/nanofibrous scaffolds electrospun from PC_ and small intestinal submucosa. Biomater. Sci., Polym. Ed. 2010; 21(5): 553-62.
  64. He W., Ma Z., Yong T. et al. Fabrication of collagen-coated biodegradable polymer nanofiber mesh and its potential for endothelial cells growth. Biomaterials 2005; 26: 7606-15.
  65. Zhu Y., Leong M.F., Ong W.F. et al. Esophageal epithelium regeneration on fibronectin grafted poly(L-lactide-co-caprolactone) (PLLC) nanofiber scaffold. Biomaterials 2007; 28: 861-8.
  66. Тенчурин Т.Х., Люндуп А.В., Демченко А.Г. и др. Модификация биодеградируемого волокнистого матрикса эпидермальным фактором роста при эмульсионном электроформовании для стимулирования пролиферации эпителиальных клеток. Гены и клетки 2017; 12(4): 47-52.
  67. _u T., _i Y., Chen T. Techniques for fabrication and construction of three-dimensional scaffolds for tissue engineering. International Journal of Nanomedicine 2013; 8: 337-50.
  68. Chua C.K., Yeong W.Y., An J. Special Issue: 3D Printing for Biomedical Engineering. Materials Basel 2017; 10(3): 243-5.
  69. Todhunter M.E., Jee N.Y., Hughes A.J. et al. Programmed synthesis of three-dimensional tissues. Nat. Methods 2015; 12(10): 975-81.
  70. Murphy W._., Peters M.C., Kohn D.H. et al. Sustained release of vascular endothelial growth factor from mineralized poly(lactide-co-glycolide) scaffolds for tissue engineering. Biomaterials 2000; 21(24): 2521-7.
  71. Moon J.J., West J._. Vascularization of engineered tissues: approaches to promote angio-genesis in biomaterials. Current topics in medicinal chemistry 2008; 8(4): 300-10.
  72. Lopes M.F., Cabrita A., Ilharco J. et al. Esophageal replacement in rat using porcine intestinal submucosa as a patch or a tubeshaped graft. Dis. Esophagus 2006; 19: 254-62.
  73. Kim B.S., Mooney D.J. Scaffolds for engineering smooth muscle under cyclic mechanical strain conditions. J. Biomech. Eng. 2000; 122(3): 210-5.
  74. Ohki T., Yamato M., Ota M. et al. Prevention of esophageal stricture after endoscopic submucosal dissection using tissue-engineered cell sheets. Gastroenterology 2012; 143: 582-8.
  75. Nieponice A., McGrath K., Qureshi I. et al. An extracellular matrix scaffold for esophageal stricture prevention after circumferential EMR. Gastrointest. Endosc. 2009; 69(2): 289-96.
  76. Agopian V.G., Chen D.C., Avansino J.R. Intestinal stem cell organoid transplantation generates neomucosa in dogs. Gastrointest. Surg. 2009; 13: 971-82.
  77. Yui S., Nakamura T., Sato T. et al. Functional engraftment of colon epithelium expanded in vitro from a single adult Lgr5+ stem cell. Nat. Med. 2012; 18: 618-23.
  78. Avansino J.R., Chen D.C., Hoagland V.D. et al. Orthotopic transplantation of intestinal mucosal organoids in rodents. Surgery 2006; 140(3): 423-34.
  79. Choi R.S., Vacanti J.P. Preliminary studies of tissue-engineered intestine using isolated epithelial organoid units on tubular synthetic biodegradable scaffolds. Transplant. Proc. 1997; 29: 848-51.
  80. Spurrier R.G., Speer A.L., Hou X. et al. Murine and Human Tissue-Engineered Esophagus Form from Sufficient Stem/Progenitor Cells and Do Not Require Microdesigned Biomaterials. Tissue Engineering Part A 2015; 21(5-6): 906-15.
  81. Vacanti J.P. Tissue and organ engineering: can we build intestine and vital organs? Gastrointest. Surg. 2003; 7(7): 831-5.
  82. Севастьянов В.И. Технологии тканевой инженерии и регенеративной медицины. Вестник трансплантологии и искусственных органов 2014; 16(3): 93-108.
  83. Вахрушев И.В., Антонов Е.Н., Суббот А.М. и др. Тканеинженерные конструкции для регенеративной медицины на основе мезенхимальных клеток пульпы молочного зуба и полимерных матриксов нового поколения. Курский научно-практический вестник «Человек и его здоровье» 2017; 2: 106-11.

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