Bioengineering kidneys for transplantation

Seminars in Nephrology

Volumn 34, Issue 4, 2014, Pages 384-393

  Madariaga, Maria Lucia L ^a,b,c   Ott, Harald C ^a,b,c  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL CANCER CENTER   (United States)

Author keywords

Bioengineering; Kidney; Organ engineering; Perfusion decellularization; Transplantation

Indexed keywords

KRUPPEL LIKE FACTOR 4; LIN28 PROTEIN; MYC PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; BIOARTIFICIAL ORGAN; BIOENGINEERING; CELL NUCLEUS TRANSPLANTATION; DEVELOPMENTAL BIOLOGY; EMBRYONIC STEM CELL; END STAGE RENAL DISEASE; EXTRACELLULAR MATRIX; EXTRACORPOREAL BIOARTIFICIAL KIDNEY; HEALTH CARE COST; HEALTH CARE NEED; HEMODIALYSIS; HUMAN; INNATE IMMUNITY; KIDNEY FUNCTION; KIDNEY GRAFT; KIDNEY TRANSPLANTATION; MEDICAL TECHNOLOGY; MESENCHYMAL STEM CELL; NEPHRON; NEUTROPHIL; PERFUSION DECELLULARIZATION TECHNIQUE; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PLURIPOTENT STEM CELL; PROTEIN EXPRESSION; QUALITY CONTROL; REGENERATIVE MEDICINE; REVIEW; STEM CELL RESEARCH; TH2 CELL; TISSUE ENGINEERING; TISSUE SCAFFOLD; XENOTRANSPLANTATION; KIDNEY; KIDNEY FAILURE, CHRONIC; PROCEDURES;

BIOENGINEERING; HUMANS; KIDNEY; KIDNEY FAILURE, CHRONIC; KIDNEY TRANSPLANTATION; TISSUE ENGINEERING;

EID: 84907996509     PISSN: 02709295     EISSN: 15584488     Source Type: Journal    
DOI: 10.1016/j.semnephrol.2014.06.005     Document Type: Review

References (99)

1. Kaiser L.R. The future of multihospital systems. Top Health Care Financ 1992, 18:32-45.
2. Dutkowski P., de Rougemont O., Clavien P.A. Alexis Carrel: genius, innovator and ideologist. Am J Transplant 2008, 8:1998-2003.
3. Orlando G., Wood K.J., Stratta R.J., Yoo J.J., Atala A., Soker S. Regenerative medicine and organ transplantation: past, present, and future. Transplantation 2011, 91:1310-1317.
4. Soto-Gutierrez A., Wertheim J.A., Ott H.C., Gilbert T.W. Perspectives on whole-organ assembly: moving toward transplantation on demand. J Clin Invest 2012, 122:3817-3823.
5. Langer R., Vacanti J.P. Tissue engineering. Science 1993, 260:920-926.
6. Orlando G., Baptista P., Birchall M., et al. Regenerative medicine as applied to solid organ transplantation: current status and future challenges. Transplant Int 2011, 24:223-232.
7. Cima L.G., Vacanti J.P., Vacanti C., Ingber D., Mooney D., Langer R. Tissue engineering by cell transplantation using degradable polymer substrates. J Biomech Eng 1991, 113:143-151.
8. Organ G.M., Mooney D.J., Hansen L.K., Schloo B., Vacanti J.P. Transplantation of enterocytes utilizing polymer-cell constructs to produce a neointestine. Transplant Proc 1992, 24:3009-3011.
9. Vacanti C.A., Langer R., Schloo B., Vacanti J.P. Synthetic polymers seeded with chondrocytes provide a template for new cartilage formation. Plast Reconstr Surg 1991, 88:753-759.
10. Fontaine M., Hansen L.K., Thompson S., et al. Transplantation of genetically altered hepatocytes using cell-polymer constructs. Transplant Proc 1993, 25:1002-1004.
11. Macchiarini P., Walles T., Biancosino C., Mertsching H. First human transplantation of a bioengineered airway tissue. J Thorac Cardiovasc Surg 2004, 128:638-641.
12. Atala A., Bauer S.B., Soker S., Yoo J.J., Retik A.B. Tissue-engineered autologous bladders for patients needing cystoplasty. Lancet 2006, 367:1241-1246.
13. L'Heureux N., McAllister T.N., de la Fuente L.M. Tissue-engineered blood vessel for adult arterial revascularization. N Engl J Med 2007, 357:1451-1453.
14. Mikos A.G., Herring S.W., Ochareon P., et al. Engineering complex tissues. Tissue Eng 2006, 12:3307-3339.
15. Jakab K., Norotte C., Marga F., Murphy K., Vunjak-Novakovic G., Forgacs G. Tissue engineering by self-assembly and bio-printing of living cells. Biofabrication 2010, 2:022001.
16. Ott H.C., Matthiesen T.S., Goh S.K., et al. Perfusion-decellularized matrix: using nature's platform to engineer a bioartificial heart. Nat Med 2008, 14:213-221.
17. Ott H.C., Clippinger B., Conrad C., et al. Regeneration and orthotopic transplantation of a bioartificial lung. Nat Med 2010, 16:927-933.
18. Petersen T.H., Calle E.A., Zhao L., et al. Tissue-engineered lungs for in vivo implantation. Science 2010, 329:538-541.
19. O'Neill J.D., Anfang R., Anandappa A., et al. Decellularization of human and porcine lung tissues for pulmonary tissue engineering. Ann Thorac Surg 2013, 96:1046-1055.
20. Baptista P.M., Orlando G., Mirmalek-Sani S.H., 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, 2009:6526-6529.
21. Nakayama K.H., Batchelder C.A., Lee C.I., Tarantal A.F. Decellularized rhesus monkey kidney as a three-dimensional scaffold for renal tissue engineering. Tissue Eng Part A 2010, 16:2207-2216.
22. Song J.J., Guyette J.P., Gilpin S.E., Gonzalez G., Vacanti J.P., Ott H.C. Regeneration and experimental orthotopic transplantation of a bioengineered kidney. Nat Med 2013, 19:646-651.
23. Uygun B.E., Soto-Gutierrez A., Yagi H., et al. Organ reengineering through development of a transplantable recellularized liver graft using decellularized liver matrix. Nat Med 2010, 16:814-820.
24. De Carlo E., Baiguera S., Conconi M.T., et al. Pancreatic acellular matrix supports islet survival and function in a synthetic tubular device: in vitro and in vivo studies. Int J Mol Med 2010, 25:195-202.
25. Campbell P.G., Weiss L.E. Tissue engineering with the aid of inkjet printers. Expert Opin Biol Ther 2007, 7:1123-1127.
26. K/DOQI clinical practice guidelines for chronic kidney disease: evaluation, classification, and stratification. Am J Kidney Dis 2002, 39(Suppl 1):S1-266. National Kidney Foundation.
27. Collins A.J., Foley R.N., Chavers B., et al. US Renal Data System 2013 annual data report. Am J Kidney Dis 2014, 63(Suppl:A7).
28. National Kidney and Urologic Diseases Information Clearinghouse (NKUDIC). A service of the National Institute of Diabetes and Digestive and Kidney Diseases (NIDDK), National Institutes of Health (NIH). [cited 2014 March 11]. Available from: http://kidney.niddk.nih.gov/kudiseases/pubs/kustats/.
29. Chertow G.M., Johansen K.L., Lew N., Lazarus J.M., Lowrie E.G. Vintage, nutritional status, and survival in hemodialysis patients. Kidney Int 2000, 57:1176-1181.
30. 2009 annual data report: atlas of end-stage renal disease in the United States 2009, USRD System. USRDS, National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases, Bethesda, MD.
31. Aebischer P., Ip T.K., Panol G., Galletti P.M. The bioartificial kidney: progress towards an ultrafiltration device with renal epithelial cells processing. Life Support Syst 1987, 5:159-168.
32. Ip T.K., Aebischer P. Renal epithelial-cell-controlled solute transport across permeable membranes as the foundation for a bioartificial kidney. Artif Organs 1989, 13:58-65.
33. Humes H.D., Weitzel W.F., Bartlett R.H., Swaniker F.C., Paganini E.P. Renal cell therapy is associated with dynamic and individualized responses in patients with acute renal failure. Blood Purif 2003, 21:64-71.
34. Humes H.D., Weitzel W.F., Bartlett R.H., et al. Initial clinical results of the bioartificial kidney containing human cells in ICU patients with acute renal failure. Kidney Int 2004, 66:1578-1588.
35. Tumlin J., Wali R., Williams W., et al. Efficacy and safety of renal tubule cell therapy for acute renal failure. J Am Soc Nephrol 2008, 19:1034-1040.
36. Chertow G.M., Waikar S.S. Toward the promise of renal replacement therapy. J Am Soc Nephrol 2008, 19:839-840.
37. Humes H.D., Buffington D., Westover A.J., Roy S., Fissell W.H. The bioartificial kidney: current status and future promise. Pediatr Nephrol 2014, 29:343-351.
38. Sanechika N., Sawada K., Usui Y., et al. Development of bioartificial renal tubule devices with lifespan-extended human renal proximal tubular epithelial cells. Nephrol Dial Transplant 2011, 26:2761-2769.
39. U.S. Department of Health and Human Services. [cited 2014 March 11]. Available from: http://organdonor.gov/about/data.html.
40. 2004 Annual Report of the U.S. Organ Procurement and Transplantation Network and the Scientific Registry of Transplant Recipients. Transplant data 1994-2003. Department of Health and Human Services, Health Resources and Services Administration, Healthcare Systems Bureau, Division of Transplantation, Rockville, MD: United Network for Organ Sharing, Richmond, VA; University Renal Research and Education Association, Ann Arbor, MI; 2004.
41. Cecka J.M. Kidney transplantation in the United States. Clin Transplant. 2008, 1-18.
42. Kahwaji J., Bunnapradist S., Hsu J.W., Idroos M.L., Dudek R. Cause of death with graft function among renal transplant recipients in an integrated healthcare system. Transplantation 2011, 91:225-230.
43. Gill J.S., Tonelli M. Penny wise, pound foolish? Coverage limits on immunosuppression after kidney transplantation. N Engl J Med 2012, 366:586-589.
44. Klein A.S., Messersmith E.E., Ratner L.E., Kochik R., Baliga P.K., Ojo A.O. Organ donation and utilization in the United States, 1999-2008. Am J Transplant 2010, 10:973-986.
45. Levenberg S., Langer R. Advances in tissue engineering. Curr Top Dev Biol 2004, 61:113-134.
46. Chiu D.T., Jeon N.L., Huang S., et al. Patterned deposition of cells and proteins onto surfaces by using three-dimensional microfluidic systems. Proc Natl Acad Sci U S A 2000, 97:2408-2413.
47. Kasko A.M., Wong D.Y. Two-photon lithography in the future of cell-based therapeutics and regenerative medicine: a review of techniques for hydrogel patterning and controlled release. Future Med Chem 2010, 2:1669-1680.
48. Fischer J., Wegener M. Ultrafast polymerization inhibition by stimulated emission depletion for three-dimensional nanolithography. Adv Mater 2012, 24:OP65-OP69.
49. Xu T., Zhao W., Zhu J.M., Albanna M.Z., Yoo J.J., Atala A. Complex heterogeneous tissue constructs containing multiple cell types prepared by inkjet printing technology. Biomaterials 2013, 34:130-139.
50. Mironov V., Boland T., Trusk T., Forgacs G., Markwald R.R. Organ printing: computer-aided jet-based 3D tissue engineering. Trends Biotechnol 2003, 21:157-161.
51. Derby B. Printing and prototyping of tissues and scaffolds. Science 2012, 338:921-926.
52. Skardal A., Mack D., Kapetanovic E., et al. Bioprinted amniotic fluid-derived stem cells accelerate healing of large skin wounds. Stem Cells Transl Med 2012, 1:792-802.
53. Gilbert T.W. Strategies for tissue and organ decellularization. J Cell Biochem 2012, 113:2217-2222.
54. Tapias L.F., Ott H.C. Decellularized scaffolds as a platform for bioengineered organs. Curr Opin Organ Transplant 2014, 19:145-152.
55. Song J.J., Ott H.C. Organ engineering based on decellularized matrix scaffolds. Trends Mol Med 2011, 17:424-432.
56. Salvatori M., Peloso A., Katari R., Orlando G. Regeneration and bioengineering of the kidney: current status and future challenges. Curr Urol Rep 2014, 15:379.
57. Nakayama K.H., Batchelder C.A., Lee C.I., Tarantal A.F. Renal tissue engineering with decellularized rhesus monkey kidneys: age-related differences. Tissue Eng Part A 2011, 17:2891-2901.
58. Burdick J.A., Vunjak-Novakovic G. Engineered microenvironments for controlled stem cell differentiation. Tissue Eng Part A 2009, 15:205-219.
59. Ross E.A., Williams M.J., Hamazaki T., et al. Embryonic stem cells proliferate and differentiate when seeded into kidney scaffolds. J Am Soc Nephrol 2009, 20:2338-2347.
60. Yang F., Williams C.G., Wang D.A., Lee H., Manson P.N., Elisseeff J. The effect of incorporating RGD adhesive peptide in polyethylene glycol diacrylate hydrogel on osteogenesis of bone marrow stromal cells. Biomaterials 2005, 26:5991-5998.
61. Silva G.A., Czeisler C., Niece K.L., et al. Selective differentiation of neural progenitor cells by high-epitope density nanofibers. Science 2004, 303:1352-1355.
62. Sokolsky-Papkov M., Agashi K., Olaye A., Shakesheff K., Domb A.J. Polymer carriers for drug delivery in tissue engineering. Adv Drug Deliv Rev 2007, 59:187-206.
63. Chen W., Shi C., Hou X., Zhang W.W., Li L. Bladder acellular matrix conjugated with basic fibroblast growth factor for bladder regeneration. Tissue Eng Part A. 2014 Jul 9, Epub ahead of print.
64. Smith P.L., Buffington D.A., Humes H.D. Kidney epithelial cells. Methods Enzymol 2006, 419:194-207.
65. Vigneau C., Polgar K., Striker G., et al. Mouse embryonic stem cell-derived embryoid bodies generate progenitors that integrate long term into renal proximal tubules in vivo. J Am Soc Nephrol 2007, 18:1709-1720.
66. Kim D., Dressler G.R. Nephrogenic factors promote differentiation of mouse embryonic stem cells into renal epithelia. J Am Soc Nephrol 2005, 16:3527-3534.
67. Xinaris C., Benedetti V., Rizzo P., et al. In vivo maturation of functional renal organoids formed from embryonic cell suspensions. J Am Soc Nephrol 2012, 23:1857-1868.
68. Thomson J.A., Itskovitz-Eldor J., Shapiro S.S., et al. Embryonic stem cell lines derived from human blastocysts. Science 1998, 282:1145-1147.
69. Gertow K., Wolbank S., Rozell B., et al. Organized development from human embryonic stem cells after injection into immunodeficient mice. Stem Cells Dev 2004, 13:421-435.
70. Batchelder C.A., Lee C.C., Matsell D.G., Yoder M.C., Tarantal A.F. Renal ontogeny in the rhesus monkey (Macaca mulatta) and directed differentiation of human embryonic stem cells towards kidney precursors. Differentiation 2009, 78:45-56.
71. Lin S.A., Kolle G., Grimmond S.M., et al. Subfractionation of differentiating human embryonic stem cell populations allows the isolation of a mesodermal population enriched for intermediate mesoderm and putative renal progenitors. Stem Cells Dev 2010, 19:1637-1648.
72. Takahashi K., Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 126:663-676.
73. Song B., Niclis J.C., Alikhan M.A., et al. Generation of induced pluripotent stem cells from human kidney mesangial cells. J Am Soc Nephrol 2011, 22:1213-1220.
74. Zhou T., Benda C., Duzinger S., et al. Generation of induced pluripotent stem cells from urine. J Am Soc Nephrol 2011, 22:1221-1228.
75. Thatava T., Armstrong A.S., De Lamo J.G., et al. Successful disease-specific induced pluripotent stem cell generation from patients with kidney transplantation. Stem Cell Res Ther 2011, 2:48.
76. Lee P.Y., Chien Y., Chiou G.Y., Lin C.H., Chiou C.H., Tarng D.C. Induced pluripotent stem cells without c-Myc attenuate acute kidney injury via downregulating the signaling of oxidative stress and inflammation in ischemia-reperfusion rats. Cell Transplant 2012, 21:2569-2585.
77. Morizane R., Monkawa T., Itoh H. Differentiation of murine embryonic stem and induced pluripotent stem cells to renal lineage in vitro. Biochem Biophys Res Commun 2009, 390:1334-1339.
78. Araoka T., Mae S., Kurose Y., et al. Efficient and rapid induction of human iPSCs/ESCs into nephrogenic intermediate mesoderm using small molecule-based differentiation methods. PLoS One 2014, 9:e84881.
79. Wise A.F., Ricardo S.D. Mesenchymal stem cells in kidney inflammation and repair. Nephrology 2012, 17:1-10.
80. de Almeida D.C., Donizetti-Oliveira C., Barbosa-Costa P., Origassa C.S., Camara N.O. In search of mechanisms associated with mesenchymal stem cell-based therapies for acute kidney injury. Clin Biochem Rev 2013, 34:131-144.
81. Choi S.J., Kim J.K., Hwang S.D. Mesenchymal stem cell therapy for chronic renal failure. Exp Opin Biol Ther 2010, 10:1217-1226.
82. Orlando G., Soker S., Stratta R.J. Organ bioengineering and regeneration as the new Holy Grail for organ transplantation. Ann Surg 2013, 258:221-232.
83. Orlando G., Di Cocco P., D'Angelo M., Clemente K., Famulari A., Pisani F. Regenerative medicine applied to solid organ transplantation: where do we stand?. Transplant Proc 2010, 42:1011-1013.
84. Folkman J., Hochberg M. Self-regulation of growth in three dimensions. J Exp Med 1973, 138:745-753.
85. Desrochers T.M., Palma E., Kaplan D.L. Tissue-engineered kidney disease models. Adv Drug Deliv Rev 2014, 69-70C:67-80.
86. Rosines E., Johkura K., Zhang X., et al. Constructing kidney-like tissues from cells based on programs for organ development: toward a method of in vitro tissue engineering of the kidney. Tissue Eng Part A 2010, 16:2441-2455.
87. Orlando G., Farney A.C., Iskandar S.S., et al. Production and implantation of renal extracellular matrix scaffolds from porcine kidneys as a platform for renal bioengineering investigations. Ann Surg 2012, 256:363-370.
88. Steer D.L., Nigam S.K. Developmental approaches to kidney tissue engineering. Am J Physiol Renal Physiol 2004, 286:F1-7.
89. Benigni A., Morigi M., Remuzzi G. Kidney regeneration. Lancet 2010, 375:1310-1317.
90. Blum B., Bar-Nur O., Golan-Lev T., Benvenisty N. The anti-apoptotic gene survivin contributes to teratoma formation by human embryonic stem cells. Nat Biotechnol 2009, 27:281-287.
91. Takahashi K., Tanabe K., Ohnuki M., et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007, 131:861-872.
92. Perin L., Da Sacco S., De Filippo R.E. Regenerative medicine of the kidney. Adv Drug Deliv Rev 2011, 63:379-387.
93. Mertsching H., Schanz J., Steger V., et al. Generation and transplantation of an autologous vascularized bioartificial human tissue. Transplantation 2009, 88:203-210.
94. Gilbert T.W., Sellaro T.L., Badylak S.F. Decellularization of tissues and organs. Biomaterials 2006, 27:3675-3683.
95. Daly K.A., Stewart-Akers A.M., Hara H., et al. Effect of the alphaGal epitope on the response to small intestinal submucosa extracellular matrix in a nonhuman primate model. Tissue Eng Part A 2009, 15:3877-3888.
96. Wainwright D.J. Use of an acellular allograft dermal matrix (AlloDerm) in the management of full-thickness burns. Burns 1995, 21:243-248.
97. Badylak S.F., Gilbert T.W. Immune response to biologic scaffold materials. Semin Immunol 2008, 20:109-116.
98. Allman A.J., McPherson T.B., Badylak S.F., et al. Xenogeneic extracellular matrix grafts elicit a TH2-restricted immune response. Transplantation 2001, 71:1631-1640.
99. Platt J.L., Cascalho M. New and old technologies for organ replacement. Curr Opin Organ Transplant 2013, 18:179-185.