Skip to main content
Top
Published in: Journal of Artificial Organs 4/2014

01-12-2014 | Review

Repopulation of decellularized whole organ scaffold using stem cells: an emerging technology for the development of neo-organ

Authors: Aleem Ahmed Khan, Sandeep Kumar Vishwakarma, Avinash Bardia, J. Venkateshwarulu

Published in: Journal of Artificial Organs | Issue 4/2014

Login to get access

Abstract

Demand of donor organs for transplantation in treatment of organ failure is increasing. Hence there is a need to develop new strategies for the alternative sources of organ development. Attempts are being made to use xenogenic organs by genetic manipulation but the organ rejection against human always has been a major challenge for the survival of the graft. Advancement in the genetic bioengineering and combination of different allied sciences for the development of humanized organ system, the therapeutic influence of stem cell fraction on the reconstitution of organ architecture and their regenerative abilities in different tissues and organs provides a better approach to solve the problem of organ shortage. However, the available strategies for generating the organ/tissue scaffolds limit its application due to the absence of complete three-dimensional (3D) organ architecture, mechanical strength, long-term cell survival, and vascularization. Repopulation of whole decellularized organ scaffolds using stem cells has added a new dimension for creating new bioengineered organs. In recent years, several studies have demonstrated the potential application of decellularization and recellularization approach for the development of functional bio-artificial organs. With the help of established procedures for conditioning, extensive stem cells and organ engineering experiments/transplants for the development of humanized organs will allow its preclinical evaluation for organ regeneration before translation to the clinic. This review focuses on the major aspects of organ scaffold generation and repopulation of different types of whole decellularized organ scaffolds using stem cells for the functional benefit and their confines.
Literature
1.
go back to reference Bailey LL, Nehlsen-Cannarella SL, Concepcion W, Jolley WB. Baboon-to-human cardiac xenotransplantation in a neonate. JAMA. 1985;254:3321–9.PubMedCrossRef Bailey LL, Nehlsen-Cannarella SL, Concepcion W, Jolley WB. Baboon-to-human cardiac xenotransplantation in a neonate. JAMA. 1985;254:3321–9.PubMedCrossRef
2.
go back to reference Lan C, Xiao W, Xiao-Hui D, Chun-Yan H, Hong-Ling Y. Tissue culture before transplantation of frozen–thawed human fetal ovarian tissue into immunodeficient mice. Fertil Steril. 2010;93:913–9.PubMedCrossRef Lan C, Xiao W, Xiao-Hui D, Chun-Yan H, Hong-Ling Y. Tissue culture before transplantation of frozen–thawed human fetal ovarian tissue into immunodeficient mice. Fertil Steril. 2010;93:913–9.PubMedCrossRef
3.
go back to reference Van Eyck AS, Bouzin C, Feron O, Romeu L, Van Langendonckt A, Donnez J, Dolmans MM. Both host and graft vessels contribute to revascularization of xenografted human ovarian tissue in a murine model. Fertil Steril. 2010;93:1676–85.PubMedCrossRef Van Eyck AS, Bouzin C, Feron O, Romeu L, Van Langendonckt A, Donnez J, Dolmans MM. Both host and graft vessels contribute to revascularization of xenografted human ovarian tissue in a murine model. Fertil Steril. 2010;93:1676–85.PubMedCrossRef
4.
go back to reference Baksh D, Davies E, Kim S. Three-dimensional matrices of calcium polyphosphates support bone growth in vitro and in vivo. J Mater Sci. 1998;9:743. Baksh D, Davies E, Kim S. Three-dimensional matrices of calcium polyphosphates support bone growth in vitro and in vivo. J Mater Sci. 1998;9:743.
5.
go back to reference Ishaug SL, Crane GM, Miller J, et al. Bone formation by three-dimensional stromal osteoblast culture in biodegradable polymer scaffolds. J Biomed Mater Res. 1997;36:17.PubMedCrossRef Ishaug SL, Crane GM, Miller J, et al. Bone formation by three-dimensional stromal osteoblast culture in biodegradable polymer scaffolds. J Biomed Mater Res. 1997;36:17.PubMedCrossRef
6.
go back to reference Ott HC, Matthiesen TS, Goh SK, Black LD, Kren SM, Netoff TI, Taylor DA. Perfusion-decellularized matrix: using nature’s platform to engineer a bioartificial heart. Nat Med. 2008;14:213–21.PubMedCrossRef Ott HC, Matthiesen TS, Goh SK, Black LD, Kren SM, Netoff TI, Taylor DA. Perfusion-decellularized matrix: using nature’s platform to engineer a bioartificial heart. Nat Med. 2008;14:213–21.PubMedCrossRef
7.
go back to reference Macchiarini P, Jungebluth P, Go T, Asnaghi MA, Rees LE, Cogan TA, Ddson A, Martorell J, Bellini S, Parnigotto PP, Dickinson SC, Hollander AP, Mantero S, Conconi MR, Birchall MA. Clinical transplantation of a tissue-engineered airway. Lancet. 2008;372:2023–30.PubMedCrossRef Macchiarini P, Jungebluth P, Go T, Asnaghi MA, Rees LE, Cogan TA, Ddson A, Martorell J, Bellini S, Parnigotto PP, Dickinson SC, Hollander AP, Mantero S, Conconi MR, Birchall MA. Clinical transplantation of a tissue-engineered airway. Lancet. 2008;372:2023–30.PubMedCrossRef
8.
go back to reference Hollander A, Macchiarini P, Gordijn B, Birchall M. The first stem cell-based tissue-engineered organ replacement: implications for regenerative medicine and society. Regen Med. 2009;4:147–8.PubMedCrossRef Hollander A, Macchiarini P, Gordijn B, Birchall M. The first stem cell-based tissue-engineered organ replacement: implications for regenerative medicine and society. Regen Med. 2009;4:147–8.PubMedCrossRef
9.
go back to reference Shackleton M, Vaillant F, Simpson KJ, Stingl J, Smyth GK, Asselin-Labat ML, Wu L, Lindeman GJ, Visvader JE. Generation of a functional mammary gland from a single stem cell. Nat. 2006;439:84–8.CrossRef Shackleton M, Vaillant F, Simpson KJ, Stingl J, Smyth GK, Asselin-Labat ML, Wu L, Lindeman GJ, Visvader JE. Generation of a functional mammary gland from a single stem cell. Nat. 2006;439:84–8.CrossRef
10.
go back to reference Stingl J, Eirew P, Ricketson I, Shackleton M, Vaillant F, Choi D, Li HI. Eaves purification and unique properties of mammary epithelial stem cells. Nat. 2006;439:993–7. Stingl J, Eirew P, Ricketson I, Shackleton M, Vaillant F, Choi D, Li HI. Eaves purification and unique properties of mammary epithelial stem cells. Nat. 2006;439:993–7.
11.
go back to reference Leong KG, Wang BE, Johnson L, Gao WQ. Generation of a prostate from a single adult stem cell. Nat. 2008;456:804–8.CrossRef Leong KG, Wang BE, Johnson L, Gao WQ. Generation of a prostate from a single adult stem cell. Nat. 2008;456:804–8.CrossRef
12.
go back to reference Chen J, Lansford R, Stewart V, Young F, Alt FW. RAG-2-deficient blastocyst complementation: an assay of gene function in lymphocyte development. Proc Natl Acad Sci USA. 1993;90:4528–32.PubMedCentralPubMedCrossRef Chen J, Lansford R, Stewart V, Young F, Alt FW. RAG-2-deficient blastocyst complementation: an assay of gene function in lymphocyte development. Proc Natl Acad Sci USA. 1993;90:4528–32.PubMedCentralPubMedCrossRef
13.
go back to reference Kobayashi T, Yamaguchi T, Hamanaka S, Kato-Itoh M, Yamazaki Y, Ibata M, Sato H, Lee YS, Usui J, Knisely AS, Hirabayashi M, Nakauchi H. Generation of rat pancreas in mouse by interspecific blastocyst injection of pluripotent stem cells. Cell. 2010;142:787–99.PubMedCrossRef Kobayashi T, Yamaguchi T, Hamanaka S, Kato-Itoh M, Yamazaki Y, Ibata M, Sato H, Lee YS, Usui J, Knisely AS, Hirabayashi M, Nakauchi H. Generation of rat pancreas in mouse by interspecific blastocyst injection of pluripotent stem cells. Cell. 2010;142:787–99.PubMedCrossRef
14.
go back to reference Cao Y, Vacanti JP, Paige KT, Upton J, Vacanti CA. Transplantation of chondrocytes utilizing a polymer-cell construct to produce tissue-engineered cartilage in the shape of a human ear. Plast Reconstr Surg. 1997;100:297–302.PubMedCrossRef Cao Y, Vacanti JP, Paige KT, Upton J, Vacanti CA. Transplantation of chondrocytes utilizing a polymer-cell construct to produce tissue-engineered cartilage in the shape of a human ear. Plast Reconstr Surg. 1997;100:297–302.PubMedCrossRef
15.
go back to reference Takebe T, Koike N, Sekine K, Enomura M, Chiba Y, Ueno Y, Zheng YW, Taniguchi H. Generation of functional human vascular network. Transpl Proc. 2012;44:1130–3.CrossRef Takebe T, Koike N, Sekine K, Enomura M, Chiba Y, Ueno Y, Zheng YW, Taniguchi H. Generation of functional human vascular network. Transpl Proc. 2012;44:1130–3.CrossRef
16.
go back to reference Badylak SF, Taylor D, Uygun K. Whole-organ tissue engineering: decellularization and recellularization of three-dimensional matrix scaffolds. Ann Rev Biomed Eng. 2011;13:27–53.CrossRef Badylak SF, Taylor D, Uygun K. Whole-organ tissue engineering: decellularization and recellularization of three-dimensional matrix scaffolds. Ann Rev Biomed Eng. 2011;13:27–53.CrossRef
17.
go back to reference Baptista PM, Orlando G, Mirmalek-Sani SH, Siddiqui M, Atala A, Soker S. Whole organ decellularization: a tool for bioscaffold fabrication and organ bioengineering. Conf Proc IEEE Eng Med Biol Soc. 2009;65:26–9. Baptista PM, Orlando G, Mirmalek-Sani SH, Siddiqui M, Atala A, Soker S. Whole organ decellularization: a tool for bioscaffold fabrication and organ bioengineering. Conf Proc IEEE Eng Med Biol Soc. 2009;65:26–9.
18.
go back to reference Habibullah CM, Vijayalakshmi V, Naseem B, Habeeb MH, Shashi S, Rao M. Hepatofunctional study of UV-B (302 nm) irradiated goat hepatocytes. Am J Gastroenterol. 2000;95:2511–2.CrossRef Habibullah CM, Vijayalakshmi V, Naseem B, Habeeb MH, Shashi S, Rao M. Hepatofunctional study of UV-B (302 nm) irradiated goat hepatocytes. Am J Gastroenterol. 2000;95:2511–2.CrossRef
19.
go back to reference Khan AA, Capoor AK, Parveen N, Naseem S, Vijayalakshmi V, Venkateshan V, Habibullah CM. In vitro studies on a bioreactor module containing encapsulated goat hepatocytes for the development of bioartificial liver. Ind J Gastroenterol. 2002;21:55–8. Khan AA, Capoor AK, Parveen N, Naseem S, Vijayalakshmi V, Venkateshan V, Habibullah CM. In vitro studies on a bioreactor module containing encapsulated goat hepatocytes for the development of bioartificial liver. Ind J Gastroenterol. 2002;21:55–8.
20.
go back to reference Ross EA, Abrahamson DR, John PL, Clapp WL, Williams MJ, et al. Mouse stem cells seeded into decellularized rat kidney scaffolds endothelialize and remodel basement membranes. Organogen. 2012;8:49–55.CrossRef Ross EA, Abrahamson DR, John PL, Clapp WL, Williams MJ, et al. Mouse stem cells seeded into decellularized rat kidney scaffolds endothelialize and remodel basement membranes. Organogen. 2012;8:49–55.CrossRef
21.
go back to reference Song JJ, Guyette JP, Gilpin SE, Gonzalez G, Vacanti JP, Ott HC. Regeneration and experimental orthotopic transplantation of a bioengineered kidney. Nat Med. 2013;19:1–8.CrossRef Song JJ, Guyette JP, Gilpin SE, Gonzalez G, Vacanti JP, Ott HC. Regeneration and experimental orthotopic transplantation of a bioengineered kidney. Nat Med. 2013;19:1–8.CrossRef
22.
go back to reference Nakayama KH, Lee CCI, Batchelder CA, Tarantal AF. Tissue specificity of decellularized rhesus monkey kidney and lung scaffolds. PLoS One. 2013;8:e64134.PubMedCentralPubMedCrossRef Nakayama KH, Lee CCI, Batchelder CA, Tarantal AF. Tissue specificity of decellularized rhesus monkey kidney and lung scaffolds. PLoS One. 2013;8:e64134.PubMedCentralPubMedCrossRef
23.
go back to reference Bowen J. By the numbers: heart transplants in the US. WSFA stories. (Online Statistics) 2012. Bowen J. By the numbers: heart transplants in the US. WSFA stories. (Online Statistics) 2012.
24.
go back to reference Ng SL, Narayanan K, Gao S, Wan AC. Lineage restricted progenitors for the repopulation of decellularized heart. Biomat. 2011;32:7571–80.CrossRef Ng SL, Narayanan K, Gao S, Wan AC. Lineage restricted progenitors for the repopulation of decellularized heart. Biomat. 2011;32:7571–80.CrossRef
25.
go back to reference Lu TY, Lin B, Kim J, Sullivan M, Tobita K, Salama G, Yang L. Repopulation of decellularized mouse heart with human induced pluripotent stem cell-derived cardiovascular progenitor cells. Nat Commun. 2013;4:2307.PubMed Lu TY, Lin B, Kim J, Sullivan M, Tobita K, Salama G, Yang L. Repopulation of decellularized mouse heart with human induced pluripotent stem cell-derived cardiovascular progenitor cells. Nat Commun. 2013;4:2307.PubMed
26.
go back to reference Zacchi V, Soranzo C, Cortivo R, Radice M, Brun P, Abatangelo G. In vitro engineering of human skin-like tissue. J Biomed Mater Res. 1998;40:187–94.PubMedCrossRef Zacchi V, Soranzo C, Cortivo R, Radice M, Brun P, Abatangelo G. In vitro engineering of human skin-like tissue. J Biomed Mater Res. 1998;40:187–94.PubMedCrossRef
27.
go back to reference Kaushal S, Amiel GE, Guleserian KJ, Shapira OM, Perry T, Sutherland FW, et al. Functional small-diameter neovessels created using endothelial progenitor cells expanded ex vivo. Nat Med. 2001;7:1035–40.PubMedCentralPubMedCrossRef Kaushal S, Amiel GE, Guleserian KJ, Shapira OM, Perry T, Sutherland FW, et al. Functional small-diameter neovessels created using endothelial progenitor cells expanded ex vivo. Nat Med. 2001;7:1035–40.PubMedCentralPubMedCrossRef
28.
go back to reference Atala A, Bauer SB, Soker S, Yoo JJ, Retik AB. Tissue-engineered autologous bladders for patients needing cystoplasty. Lancet. 2006;367:1241–6.PubMedCrossRef Atala A, Bauer SB, Soker S, Yoo JJ, Retik AB. Tissue-engineered autologous bladders for patients needing cystoplasty. Lancet. 2006;367:1241–6.PubMedCrossRef
29.
go back to reference Griffith LG, Naughton G. Tissue engineering—current challenges and expanding opportunities. Sci. 2002;295:1009–14.CrossRef Griffith LG, Naughton G. Tissue engineering—current challenges and expanding opportunities. Sci. 2002;295:1009–14.CrossRef
30.
go back to reference Baptista PM, Siddiqui MM, Lozier G, Rodriguez SR, Atala A, Soker S. The use of whole organ decellularization for the generation of a vascularized liver organoid. Hepatol. 2011;53:604–17.CrossRef Baptista PM, Siddiqui MM, Lozier G, Rodriguez SR, Atala A, Soker S. The use of whole organ decellularization for the generation of a vascularized liver organoid. Hepatol. 2011;53:604–17.CrossRef
32.
go back to reference Rogers SA, Hammerman MR. Prolongation of life in anephric rats following de novo renal organogenesis. Organogen. 2004;1:22–5.CrossRef Rogers SA, Hammerman MR. Prolongation of life in anephric rats following de novo renal organogenesis. Organogen. 2004;1:22–5.CrossRef
33.
35.
go back to reference Lopez AD, Shibuya K, Rao C, et al. Chronic obstructive pulmonary disease: current burden and future projections. Eur Respir J. 2006;27:397–412.PubMedCrossRef Lopez AD, Shibuya K, Rao C, et al. Chronic obstructive pulmonary disease: current burden and future projections. Eur Respir J. 2006;27:397–412.PubMedCrossRef
36.
go back to reference Eisner MD, Anthonisen N, Coultas D, et al. An official American thoracic society public policy statement: novel risk factors and the global burden of chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2010;182:693–718.PubMedCrossRef Eisner MD, Anthonisen N, Coultas D, et al. An official American thoracic society public policy statement: novel risk factors and the global burden of chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2010;182:693–718.PubMedCrossRef
37.
go back to reference Cortiella J, Niles J, Cantu A, et al. Influence of acellular natural lung matrix on murine embryonic stem cell differentiation and tissue formation. Tissue Eng Part A. 2010;16:2565–80.PubMedCrossRef Cortiella J, Niles J, Cantu A, et al. Influence of acellular natural lung matrix on murine embryonic stem cell differentiation and tissue formation. Tissue Eng Part A. 2010;16:2565–80.PubMedCrossRef
38.
go back to reference Petersen TH, et al. Tissue-engineered lungs for in vivo implantation. Sci. 2010;329:538–41.CrossRef Petersen TH, et al. Tissue-engineered lungs for in vivo implantation. Sci. 2010;329:538–41.CrossRef
39.
go back to reference Price AP, England KA, et al. Development of a decellularized lung bioreactor system for bioengineering the lung: the matrix reloaded. Tissue Eng Part A. 2010;16:2581–91.PubMedCentralPubMedCrossRef Price AP, England KA, et al. Development of a decellularized lung bioreactor system for bioengineering the lung: the matrix reloaded. Tissue Eng Part A. 2010;16:2581–91.PubMedCentralPubMedCrossRef
40.
go back to reference Petersen TH, Calle EA, Colehour MB, et al. Matrix composition and mechanics of decellularized lung scaffolds. Cells Tissue Org. 2012;195:222–31.CrossRef Petersen TH, Calle EA, Colehour MB, et al. Matrix composition and mechanics of decellularized lung scaffolds. Cells Tissue Org. 2012;195:222–31.CrossRef
41.
go back to reference Osada H, Takeuchi S, Kojima K, Yamate N. The first step of experimental study on hybrid trachea: use of cultured fibroblasts with artificial matrix. J Cardiovasc Surg (Torino). 1994;35:165–8. Osada H, Takeuchi S, Kojima K, Yamate N. The first step of experimental study on hybrid trachea: use of cultured fibroblasts with artificial matrix. J Cardiovasc Surg (Torino). 1994;35:165–8.
42.
go back to reference Vacanti CA, Paige KT, Kim WS, Sakata J, Upton J, et al. Experimental tracheal replacement using tissue-engineered cartilage. J Pediatr Surg. 1994;29:201–4.PubMedCrossRef Vacanti CA, Paige KT, Kim WS, Sakata J, Upton J, et al. Experimental tracheal replacement using tissue-engineered cartilage. J Pediatr Surg. 1994;29:201–4.PubMedCrossRef
43.
go back to reference Paz AC, Kojima K, Iwasaki K, Ross JD, Canseco JA, et al. Tissue engineered trachea using decellularized aorta. J Bioeng Biomed Sci. 2011;S2:001. Paz AC, Kojima K, Iwasaki K, Ross JD, Canseco JA, et al. Tissue engineered trachea using decellularized aorta. J Bioeng Biomed Sci. 2011;S2:001.
44.
go back to reference DeQuach JA, et al. Simple and high yielding method for preparing tissue specific extracellular matrix coatings for cell culture. PLoS One. 2010;5:e13039.PubMedCentralPubMedCrossRef DeQuach JA, et al. Simple and high yielding method for preparing tissue specific extracellular matrix coatings for cell culture. PLoS One. 2010;5:e13039.PubMedCentralPubMedCrossRef
45.
go back to reference Ott HC, Clippinger B, Conrad C, Schuetz C, Pomerantseva I, Ikonomou L, Kotton D, Vacanti JP. Regeneration and orthotopic transplantation of a bioartificial lung. Nat Med. 2010;16:927–33.PubMedCrossRef Ott HC, Clippinger B, Conrad C, Schuetz C, Pomerantseva I, Ikonomou L, Kotton D, Vacanti JP. Regeneration and orthotopic transplantation of a bioartificial lung. Nat Med. 2010;16:927–33.PubMedCrossRef
46.
go back to reference Brown BN, Freund JM, Han LI, Rubin JP, Reing JE, et al. Comparison of three methods for the derivation of a biological scaffold composed of adipose tissue extracellular matrix. Tissue Eng. 2011;17:411–21.CrossRef Brown BN, Freund JM, Han LI, Rubin JP, Reing JE, et al. Comparison of three methods for the derivation of a biological scaffold composed of adipose tissue extracellular matrix. Tissue Eng. 2011;17:411–21.CrossRef
47.
go back to reference Gilbert TW, Sellaro TL, Badylak SF. Decellularization of tissues and organs. Biomat. 2006;27:3675–83. Gilbert TW, Sellaro TL, Badylak SF. Decellularization of tissues and organs. Biomat. 2006;27:3675–83.
48.
go back to reference Gupta SK, Dinda AK, Potdar PD, Mishra NC. Modification of decellularized goat-lung scaffold with chitosan/nanohydroxyapatite composite for bone tissue engineering applications. BioMed Res Internat 2013;2013:1–11.CrossRef Gupta SK, Dinda AK, Potdar PD, Mishra NC. Modification of decellularized goat-lung scaffold with chitosan/nanohydroxyapatite composite for bone tissue engineering applications. BioMed Res Internat 2013;2013:1–11.CrossRef
49.
go back to reference Sano MB, Neal RE, Garcia PA, Gerber D, Robertson J, Davalos RV. Towards the creation of decellularized organ constructs using irreversible electroporation and active mechanical perfusion. Biomed Eng Online. 2010;9:83.PubMedCentralPubMedCrossRef Sano MB, Neal RE, Garcia PA, Gerber D, Robertson J, Davalos RV. Towards the creation of decellularized organ constructs using irreversible electroporation and active mechanical perfusion. Biomed Eng Online. 2010;9:83.PubMedCentralPubMedCrossRef
50.
go back to reference Shupe T, Williams M, Brown A, Willenberg B, Petersen BE. Methods for the decellularization of intact rat liver. Organogen. 2010;6:134–6.CrossRef Shupe T, Williams M, Brown A, Willenberg B, Petersen BE. Methods for the decellularization of intact rat liver. Organogen. 2010;6:134–6.CrossRef
Metadata
Title
Repopulation of decellularized whole organ scaffold using stem cells: an emerging technology for the development of neo-organ
Authors
Aleem Ahmed Khan
Sandeep Kumar Vishwakarma
Avinash Bardia
J. Venkateshwarulu
Publication date
01-12-2014
Publisher
Springer Japan
Published in
Journal of Artificial Organs / Issue 4/2014
Print ISSN: 1434-7229
Electronic ISSN: 1619-0904
DOI
https://doi.org/10.1007/s10047-014-0780-2

Other articles of this Issue 4/2014

Journal of Artificial Organs 4/2014 Go to the issue