The immune boundaries for stem cell based therapies: Problems and prospective solutions

Journal of Cellular and Molecular Medicine

Volumn 13, Issue 8 A, 2009, Pages 1464-1475

  Hmadcha, Abdelkrim ^a   Domínguez Bendala, Juan ^b   Wakeman, Jane ^c   Arredouani, Mohamed ^d   Soria, Bernat ^a  

^a CABIMER Andalusian Center for Molecular Biology and Regenerative Medicine CSIC University of Seville UPO   (Spain)

^b UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^c BANGOR UNIVERSITY   (United Kingdom)

^d BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

Cell therapies; Histocompatibility; Immune rejection; Stem cells

Indexed keywords

ANIMAL; ARTICLE; CLASSIFICATION; CYTOLOGY; GRAFT REJECTION; HISTOCOMPATIBILITY; HUMAN; IMMUNE SYSTEM; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; METHODOLOGY; STEM CELL; STEM CELL TRANSPLANTATION;

ANIMALS; GRAFT REJECTION; HISTOCOMPATIBILITY; HUMANS; IMMUNE SYSTEM; IMMUNE TOLERANCE; STEM CELL TRANSPLANTATION; STEM CELLS;

EID: 70349303624     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2009.00837.x     Document Type: Article

References (182)

1. Thomson JA, Itskovitz-Eldor J, Shapiro SS, et al. Embryonic stem cell lines derived from human blastocysts. Science. 1998 282 : 1145 1147.
2. Garcia-Olmo D, Garcia-Arranz M, Herreros D, et al. A phase I clinical trial of the treatment of Crohn's fistula by adipose mesenchymal stem cell transplantation. Dis Colon Rectum. 2005 48 : 1416 1423.
3. Fortun PJ, Hawkey CJ. The role of stem cell transplantation in inflammatory bowel disease. Autoimmunity. 2008 41 : 654 659.
4. Lanzoni G, Roda G, Belluzzi A, et al. Inflammatory bowel disease: moving toward a stem cell-based therapy. World J Gastroenterol. 2008 14 : 4616 4626.
5. Assmus B, Honold J, Schachinger V, et al. Transcoronary transplantation of progenitor cells after myocardial infarction. N Engl J Med. 2006 355 : 1222 1232. (Pubitemid 44427446)
6. Schachinger V, Erbs S, Elsasser A, et al. Intracoronary bone marrow-derived progenitor cells in acute myocardial infarction. N Engl J Med. 2006 355 : 1210 1221. (Pubitemid 44427445)
7. Fang B, Song YP, Liao LM, et al. Treatment of severe therapy-resistant acute graft-versus-host disease with human adipose tissue-derived mesenchymal stem cells. Bone Marrow Transplant. 2006 38 : 389 390.
8. Le Blanc K, Rasmusson I, Sundberg B, et al. Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet. 2004 363 : 1439 1441.
9. Burt RK, Marmont A, Oyama Y, et al. Randomized controlled trials of autologous hematopoietic stem cell transplantation for autoimmune diseases: the evolution from myeloablative to lymphoablative transplant regimens. Arthritis Rheum. 2006 54 : 3750 3760.
10. Voltarelli JC, Couri CE, Stracieri AB, et al. Autologous nonmyeloablative hematopoietic stem cell transplantation in newly diagnosed type 1 diabetes mellitus. JAMA. 2007 297 : 1568 1576.
11. Kabelitz D, Geissler EK, Soria B, et al. Toward cell-based therapy of type I diabetes. Trends Immunol. 2008 29 : 68 74.
12. Tateishi-Yuyama E, Matsubara H, Murohara T, et al. Therapeutic angiogenesis for patients with limb ischaemia by autologous transplantation of bone-marrow cells: a pilot study and a randomised controlled trial. Lancet. 2002 360 : 427 435.
13. Chen Z, Palmer TD. Cellular repair of CNS disorders: an immunological perspective. Hum Mol Genet. 2008 17 : R84 92.
14. Otani A, Dorrell MI, Kinder K, et al. Rescue of retinal degeneration by intravitreally injected adult bone marrow-derived lineage-negative hematopoietic stem cells. J Clin Invest. 2004 114 : 765 774.
15. Barberi T, Klivenyi P, Calingasan NY et al. Neural subtype specification of fertilization and nuclear transfer embryonic stem cells and application in parkinsonian mice. Nat Biotechnol. 2003 21 : 1200 1207.
16. Bjorklund LM, Sanchez-Pernaute R, Chung S, et al. Embryonic stem cells develop into functional dopaminergic neurons after transplantation in a Parkinson rat model. Proc Natl Acad Sci USA. 2002 99 : 2344 2349.
17. Sonntag KC, Sanchez-Pernaute R. Tailoring human embryonic stem cells for neurodegenerative disease therapy. Curr Opin Investig Drugs. 2006 7 : 614 618.
18. Spitere K, Toulouse A, O'Sullivan DB et al. TAT-PAX6 protein transduction in neural progenitor cells: a novel approach for generation of dopaminergic neurones in vitro. Brain Res. 2008 1208 : 25 34.
19. Svendsen C. Stem cells and Parkinson's disease: toward a treatment, not a cure. Cell Stem Cell. 2008 2 : 412 413.
20. Brustle O, Jones KN, Learish RD, et al. Embryonic stem cell-derived glial precursors: a source of myelinating transplants. Science. 1999 285 : 754 756.
21. Darabi R, Gehlbach K, Bachoo RM, et al. Functional skeletal muscle regeneration from differentiating embryonic stem cells. Nat Med. 2008 14 : 134 143.
22. Darabi R, Santos FN, Perlingeiro RC. The therapeutic potential of embryonic and adult stem cells for skeletal muscle regeneration. Stem Cell Rev. 2008 4 : 217 225.
23. Klug MG, Soonpaa MH, Field LJ. DNA synthesis and multinucleation in embryonic stem cell-derived cardiomyocytes. Am J Physiol. 1995 269 : H1913 21.
24. Klug MG, Soonpaa MH, Koh GY, et al. Genetically selected cardiomyocytes from differentiating embronic stem cells form stable intracardiac grafts. J Clin Invest. 1996 98 : 216 224.
25. Laflamme MA, Chen KY, Naumova AV, et al. Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat Biotechnol. 2007 25 : 1015 1024.
26. Kehat I, Khimovich L, Caspi O, et al. Electromechanical integration of cardiomyocytes derived from human embryonic stem cells. Nat Biotechnol. 2004 22 : 1282 1289. (Pubitemid 39341201)
27. Kroon E, Martinson LA, Kadoya K, et al. Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo. Nat Biotechnol. 2008 26 : 443 452.
28. D'Amour KA, Bang AG, Eliazer S, et al. Production of pancreatic hormone-expressing endocrine cells from human embryonic stem cells. Nat Biotechnol. 2006 24 : 1392 1401.
29. Leon-Quinto T, Jones J, Skoudy A, et al. In vitro directed differentiation of mouse embryonic stem cells into insulin-producing cells. Diabetologia. 2004 47 : 1442 1451. (Pubitemid 39232431)
30. Soria B, Roche E, Berna G, et al. Insulin-secreting cells derived from embryonic stem cells normalize glycemia in strepto-zotocin-induced diabetic mice. Diabetes. 2000 49 : 157 162.
31. Vaca P, Martin F, Vegara-Meseguer JM, et al. Induction of differentiation of embryonic stem cells into insulin-secreting cells by fetal soluble factors. Stem Cells. 2006 24 : 258 265.
32. Bieberich E, Silva J, Wang G, et al. Selective apoptosis of pluripotent mouse and human stem cells by novel ceramide analogues prevents teratoma formation and enriches for neural precursors in ES cell-derived neural transplants. J Cell Biol. 2004 167 : 723 734.
33. Fujikawa T, Oh SH, Pi L, et al. Teratoma formation leads to failure of treatment for type I diabetes using embryonic stem cell-derived insulin-producing cells. Am J Pathol. 2005 166 : 1781 1791.
34. Joffre O, Santolaria T, Calise D, et al. Prevention of acute and chronic allograft rejection with CD4+CD25+Foxp3+ regulatory T lymphocytes. Nat Med. 2008 14 : 88 92.
35. Scandling JD, Busque S, Dejbakhsh-Jones S, et al. Tolerance and chimerism after renal and hematopoietic-cell transplantation. N Engl J Med. 2008 358 : 362 368.
36. Swijnenburg RJ, Schrepfer S, Govaert JA, et al. Immunosuppressive therapy mitigates immunological rejection of human embryonic stem cell xenografts. Proc Natl Acad Sci USA. 2008 105 : 12991 12996.
37. Chidgey AP, Boyd RL. Immune privilege for stem cells: not as simple as it looked. Cell Stem Cell. 2008 3 : 357 358.
38. Sutherland JS, Spyroglou L, Muirhead JL, et al. Enhanced immune system regeneration in humans following allogeneic or autologous hemopoietic stem cell transplantation by temporary sex steroid blockade. Clin Cancer Res. 2008 14 : 1138 1149.
39. Waldmann H, Cobbold S. Exploiting tolerance processes in transplantation. Science. 2004 305 : 209 212.
40. Carpenter MK, Rosier ES, Fisk GJ, et al. Properties of four human embryonic stem cell lines maintained in a feeder-free culture system. Dev Dyn. 2004 229 : 243 258.
41. Festag M, Sehner C, Steinberg P, et al. An in vitro embryotoxicity assay based on the disturbance of the differentiation of murine embryonic stem cells into endothelial cells. I: establishment of the differentiation protocol. Toxicol In Vitro. 2007 21 : 1619 1630. (Pubitemid 350086873)
42. Fico A, Manganelli G, Simeone M, et al. High-throughput screening-compatible single-step protocol to differentiate embryonic stem cells in neurons. Stem Cells Dev. 2008 17 : 573 584.
43. Dimos JT, Rodolfa KT, Niakan KK, et al. Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science. 2008 321 : 1218 1221.
44. Park IH, Arora N, Huo H, et al. Disease-specific induced pluripotent stem cells. Cell. 2008 134 : 877 886.
45. Evans MJ, Kaufman MH. Establishment in culture of pluripotential cells from mouse embryos. Nature. 1981 292 : 154 156.
46. Martin GR. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci USA. 1981 78 : 7634 7638.
47. Capecchi MR. Altering the genome by homologous recombination. Science. 1989 244 : 1288 1292.
48. Campbell KH, McWhir J, Ritchie WA, et al. Sheep cloned by nuclear transfer from a cultured cell line. Nature. 1996 380 : 64 6.
49. Wilmut I, Schnieke AE, McWhir J, et al. Viable offspring derived from fetal and adult mammalian cells. Nature. 1997 385 : 810 813.
50. McCreath KJ, Howcroft J, Campbell KH, et al. Production of gene-targeted sheep by nuclear transfer from cultured somatic cells. Nature. 2000 405 : 1066 1069.
51. Thomson JA, Marshall VS. Primate embryonic stem cells. Curr Top Dev Biol. 1998 38 : 133 165.
52. Bhattacharya B, Miura T, Brandenberger R, et al. Gene expression in human embryonic stem cell lines: unique molecular signature. Blood. 2004 103 : 2956 2964.
53. Boyer LA, Lee TI, Cole MF, et al. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell. 2005 122 : 947 956.
54. Amit M, Carpenter MK, Inokuma MS et al. Clonally derived human embryonic stem cell lines maintain pluripotency and proliferative potential for prolonged periods of culture. Dev Biol. 2000 227 : 271 278.
55. Cowan CA, Klimanskaya I, McMahon J et al. Derivation of embryonic stem-cell lines from human blastocysts. N Engl J Med. 2004 350 : 1353 1356.
56. Hori Y, Rulifson IC, Tsai BC, et al. Growth inhibitors promote differentiation of insulin-producing tissue from embryonic stem cells. Proc Natl Acad Sci USA. 2002 99 : 16105 16110.
57. Odorico JS, Kaufman DS, Thomson JA. Multilineage differentiation from human embryonic stem cell lines. Stem Cells. 2001 19 : 193 204.
58. Vogel G. Cell biology. Ready or not? Human ES cells head toward the clinic. Science. 2005 308 : 1534 1538.
59. Fareed MU, Moolten FL. Suicide gene transduction sensitizes murine embryonic and human mesenchymal stem cells to ablation on demand - a fail-safe protection against cellular misbehavior. Gene Ther. 2002 9 : 955 962.
60. Schuldiner M, Itskovitz-Eldor J, Benvenisty N. Selective ablation of human embryonic stem cells expressing a "suicide" gene. Stem Cells. 2003 21 : 257 265.
61. Tamada K, Wang XP, Brunicardi FC. Molecular targeting of pancreatic disorders. World J Surg. 2005 29 : 325 333.
62. Wang XP, Yazawa K, Yang J, et al. Specific gene expression and therapy for pancreatic cancer using the cytosine deaminase gene directed by the rat insulin promoter. J Gastrointest Surg. 2004 8 : 98 108.
63. Yazawa K, Fisher WE, Brunicardi FC. Current progress in suicide gene therapy for cancer. World J Surg. 2002 26 : 783 789.
64. Carpenter MK, Rosler E, Rao MS. Characterization and differentiation of human embryonic stem cells. Cloning Stem Cells. 2003 5 : 79 88.
65. Rosler ES, Fisk GJ, Ares X, et al. Long-term culture of human embryonic stem cells in feeder-free conditions. Dev Dyn. 2004 229 : 259 274.
66. Imreh MP, Gertow K, Cedervall J, et al. In vitro culture conditions favoring selection of chromosomal abnormalities in human ES cells. J Cell Biochem. 2006 99 : 508 516.
67. Baker DE, Harrison NJ, Maltby E, et al. Adaptation to culture of human embryonic stem cells and oncogenesis in vivo. Nat Biotechnol. 2007 25 : 207 215.
68. Borstlap J, Kurtz A, Stacey G, et al. Development of a European human embryonic stem cell registry. Regen Med. 2008 3 : 945 951.
69. Hyun I, Lindvall O, Ahrlund-Richter L et al. New ISSCR guidelines underscore major principles for responsible transla-tional stem cell research. Cell Stem Cell. 2008 3 : 607 609.
70. Wadman M. Stem cells ready for prime time. Nature. 2009 457 : 516.
71. Anderson DJ, Gage FH, Weissman IL. Can stem cells cross lineage boundaries? Nat Med. 2001 7 : 393 395.
72. van der Kooy D, Weiss S. Why stem cells? Science. 2000 287 : 1439 1441.
73. Dominici M, Le Blanc K, Mueller I, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006 8 : 315 317.
74. Verfaillie CM. Multipotent adult progenitor cells: an update. Novartis Found Symp. 2005 265 : 55 61.
75. Horwitz EM, Le Blanc K, Dominici M, et al. Clarification of the nomenclature for MSC: The International Society for Cellular Therapy position statement. Cytotherapy. 2005 7 : 393 395.
76. D'Ippolito G, Diabira S, Howard GA, et al. Low oxygen tension inhibits osteogenic differentiation and enhances stemness of human MIAMI cells. Bone. 2006 39 : 513 522.
77. D'Ippolito G, Howard GA, Roos BA, et al. Isolation and characterization of marrow-isolated adult multilineage inducible (MIAMI) cells. Exp Hematol. 2006 34 : 1608 1610.
78. Liedtke S, Stephan M, Kogler G. Oct4 expression revisited: potential pitfalls for data misinterpretation in stem cell research. Biol Chem. 2008 389 : 845 850.
79. Wu Y, Chen L, Scott PG, et al. Mesenchymal stem cells enhance wound healing through differentiation and angio-genesis. Stem Cells. 2007 25 : 2648 2659.
80. Wu Y, Wang J, Scott PG, et al. Bone marrow-derived stem cells in wound healing: a review. Wound Repair Regen. 2007 15 : S18 26.
81. Hare JM, Chaparro SV. Cardiac regeneration and stem cell therapy. Curr Opin Organ Transplant. 2008 13 : 536 542.
82. Abdi R, Fiorina P, Adra CN, et al. Immunomodulation by mesenchymal stem cells: a potential therapeutic strategy for type 1 diabetes. Diabetes. 2008 57 : 1759 1767.
83. Le Blanc K, Ringden O. Immuno-modulation by mesenchymal stem cells and clinical experience. J Intern Med. 2007 262 : 509 525. (Pubitemid 47620502)
84. Mishra PK. Bone marrow-derived mesenchymal stem cells for treatment of heart failure: is it all paracrine actions and immunomodulation? J Cardiovasc Med. 2008 9 : 122 128.
85. Ozaki K, Sato K, Oh I, et al. Mechanisms of immunomodulation by mesenchymal stem cells. Int J Hematol. 2007 86 : 5 7.
86. Ball SG, Shuttleworth CA, Kielty CM. Mesenchymal stem cells and neovascularization: role of platelet-derived growth factor receptors. J Cell Mol Med. 2007 11 : 1012 1030.
87. Sadat S, Gehmert S, Song YH, et al. The cardioprotective effect of mesenchymal stem cells is mediated by IGF-I and VEGF. Biochem Biophys Res Commun. 2007 363 : 674 679.
88. Ball LM, Bernardo ME, Roelofs H, et al. Cotransplantation of ex vivo expanded mesenchymal stem cells accelerates lymphocyte recovery and may reduce the risk of graft failure in haploidentical hematopoietic stem-cell transplantation. Blood. 2007 110 : 2764 2767.
89. Johansson U, Rasmusson I, Niclou SP et al. Formation of composite endothelial cell-mesenchymal stem cell islets: a novel approach to promote islet revascularization. Diabetes. 2008 57 : 2393 2401.
90. Fang B, Li N, Song Y, et al. Cotransplantation of haploidentical mesenchymal stem cells to enhance engraft-ment of hematopoietic stem cells and to reduce the risk of graft failure in two children with severe aplastic anemia. Pediatr Transplant. 2009 13 : 499 502.
91. Lee ST, Maeng H, Chwae YJ, et al. Effect of mesenchymal stem cell transplantation on the engraftment of human hematopoietic stem cells and leukemic cells in mice model. Int J Hematol. 2008 87 : 327 337.
92. Noort WA, Kruisselbrink AB, in't Anker PS, et al. Mesenchymal stem cells promote engraftment of human umbilical cord blood-derived CD34(+) cells in NOD/SCID mice. Exp Hematol. 2002 30 : 870 878.
93. Becker AJ, McCulloch EA, Till JE. Cytological demonstration of the clonal nature of spleen colonies derived from transplanted mouse marrow cells. Nature. 1963 197 : 452 454.
94. Morrison SJ, Uchida N, Weissman IL. The biology of hematopoietic stem cells. Annu Rev Cell Dev Biol. 1995 11 : 35 71.
95. Hong DS, Deeg HJ. Hemopoietic stem cells: sources and applications. Med Oncol. 1994 11 : 63 8.
96. Harris DT, Badowski M, Ahmad N, et al. The potential of cord blood stem cells for use in regenerative medicine. Expert Opin Biol Ther. 2007 7 : 1311 1322.
97. Harris DT, Rogers I. Umbilical cord blood: a unique source of pluripotent stem cells for regenerative medicine. Curr Stem Cell Res Ther. 2007 2 : 301 309.
98. Iskovich S, Kaminitz A, Yafe MP, et al. Participation of adult bone marrow-derived stem cells in pancreatic regeneration: neo-genesis versus endogenesis. Curr Stem Cell Res Ther. 2007 2 : 272 279.
99. Polgar K, Adany R, Abel G, et al. Characterization of rapidly adhering amniotic fluid cells by combined immunofluo-rescence and phagocytosis assays. Am J Hum Genet. 1989 45 : 786 792.
100. Priest RE, Marimuthu KM, Priest JH. Origin of cells in human amniotic fluid cultures: ultrastructural features. Lab Invest. 1978 39 : 106 109.
101. De Coppi P, Bartsch G Jr., Siddiqui MM, et al. Isolation of amniotic stem cell lines with potential for therapy. Nat Biotechnol. 2007 25 : 100 106.
102. Sarićc T, Frenzel L P, Hescheler J. Immunological barriers to embryonic stem cell-derived therapies. Cells Tissues Organs. 2008 188 : 78 90.
103. Daley GQ, Scadden DT. Prospects for stem cell-based therapy. Cell. 2008 132 : 544 548.
104. Deb KD, Sarda K. Human embryonic stem cells: preclinical perspectives. J Transl Med. 2008 6 : 7.
105. Carlsson PO, Mattsson G. Oxygen tension and blood flow in relation to revascularization in transplanted adult and fetal rat pancreatic islets. Cell Transplant. 2002 11 : 813 820.
106. Roh JK, Jung KH, Chu K. Adult stem cell transplantation in stroke: its limitations and prospects. Curr Stem Cell Res Ther. 2008 3 : 185 196.
107. Hwang WS, Lee BC, Lee CK, et al. Cloned human embryonic stem cells for tissue repair and transplantation. Stem Cell Rev. 2005 1 : 99 109.
108. Hwang WS, Roh SI, Lee BC, et al. Patient-specific embryonic stem cells derived from human SCNT blastocysts. Science. 2005 308 : 1777 1783.
109. Hwang WS, Ryu YJ, Park JH, et al. Evidence of a pluripotent human embryonic stem cell line derived from a cloned blastocyst. Science. 2004 303 : 1669 1674.
110. Kennedy D. Editorial retraction. Science. 2006 311 : 335.
111. French AJ, Adams CA, Anderson LS, et al. Development of human cloned blastocysts following somatic cell nuclear transfer (SCNT) with adult fibroblasts. Stem Cells. 2008 26 : 485 493.
112. Collas P. Nuclear reprogramming in cell-free extracts. Philos Trans R Soc Lond B Biol Sci. 2003 358 : 1389 1395.
113. Collas P, Taranger CK. Epigenetic reprogramming of nuclei using cell extracts. Stem Cell Rev. 2006 2 : 309 317.
114. Collas P, Taranger CK. Toward reprogramming cells to pluripotency. Ernst Schering Res Found Workshop. 2006 47 67.
115. Collas P, Taranger CK, Boquest AC, et al. On the way to reprogramming cells to pluripotency using cell-free extracts. Reprod Biomed Online. 2006 12 : 762 770.
116. Cowan CA, Atienza J, Melton DA, et al. Nuclear reprogramming of somatic cells after fusion with human embryonic stem cells. Science. 2005 309 : 1369 1373.
117. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006 126 : 663 676.
118. 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.
119. Yu J, Vodyanik MA, Smuga-Otto K, et al. Induced pluripotent stem cell lines derived from human somatic cells. Science. 2007 318 : 1917 1920.
120. Hanna J, Wernig M, Markoulaki S, et al. Treatment of sickle cell anemia mouse model with iPS cells generated from autol-ogous skin. Science. 2007 318 : 1920 1923.
121. Okita K, Ichisaka T, Yamanaka S. Generation of germline-competent induced pluripotent stem cells. Nature. 2007 448 : 313 317.
122. Okita K, Nakagawa M, Hyenjong H, et al. Generation of mouse induced pluripotent stem cells without viral vectors. Science. 2008 322 : 949 953.
123. Stadtfeld M, Nagaya M, Utikal J, et al. Induced pluripotent stem cells generated without viral integration. Science. 2008 322 : 945 949.
124. Moore KE, Mills JF, Thornton MM. Alternative sources of adult stem cells: a possible solution to the embryonic stem cell debate. Gend Med. 2006 3 : 161 168.
125. Bradley JA, Bolton EM, Pedersen RA. Stem cell medicine encounters the immune system. Nat Rev Immunol. 2002 2 : 859 871.
126. Drukker M, Katz G, Urbach A, et al. Characterization of the expression of MHC proteins in human embryonic stem cells. Proc Natl Acad Sci USA. 2002 99 : 9864 9869. (Pubitemid 34831138)
127. Draper JS, Pigott C, Thomson JA, Andrews PW. Surface antigens of human embryonic stem cells: changes upon differentiation in culture. J Anat. 2002 200 : 249 258.
128. Drukker M, Katchman H, Katz G, et al. Human embryonic stem cells and their differentiated derivatives are less susceptible to immune rejection than adult cells. Stem Cells. 2006 24 : 221 229.
129. Grinnemo KH, Kumagai-Braesch M, Mansson-Broberg A, et al. Human embryonic stem cells are immunogenic in allo-geneic and xenogeneic settings. Reprod Biomed Online. 2006 13 : 712 724.
130. Simpson E, Scott D, James E, et al. Minor H antigens: genes and peptides. Eur J Immunogenet. 2001 28 : 505 513.
131. Cooper DK. Clinical survey of heart transplantation between ABO blood group-incompatible recipients and donors. J Heart Transplant. 1990 9 : 376 381.
132. Atoui R, Asenjo JF, Duong M, et al. Marrow stromal cells as universal donor cells for myocardial regenerative therapy: their unique immune tolerance. Ann Thorac Surg. 2008 85 : 571 579.
133. Gajewski JL, Johnson VV, Sandler SG, et al. A review of transfusion practice before, during, and after hematopoietic progenitor cell transplantation. Blood. 2008 112 : 3036 3047.
134. Appleman LJ, Boussiotis VA. T cell anergy and costimulation. Immunol Rev. 2003 192 : 161 180.
135. Dugast AS, Vanhove B. Immune regulation by non-lymphoid cells in transplantation. Clin Exp Immunol. 2009 156 : 25 34.
136. Haeryfar SM, Lan Z, Leon-Ponte M, et al. Prolongation of cardiac allograft survival by rapamycin and the invariant natural killer T cell glycolipid agonist OCH. Transplantation. 2008 86 : 460 468.
137. Yu J, Venstrom JM, Liu XR, et al. Breaking tolerance to self, circulating natural killer cells expressing inhibitory KIR for non-self HLA exhibit effector function following T-cell depleted allogeneic hematopoietic cell transplantation. Blood. 2009 113 : 3875 3884.
138. Wakao H, Wakao R, Sakata S, et al. In vitro induction of natural killer T cells from embryonic stem cells prepared using somatic cell nuclear transfer. FASEB J. 2008 22 : 2223 2231.
139. Miki T, Lehmann T, Cai H, et al. Stem cell characteristics of amniotic epithelial cells. Stem Cells. 2005 23 : 1549 1559.
140. Miki T, Strom SC. Amnion-derived pluripotent/multipotent stem cells. Stem Cell Rev. 2006 2 : 133 142.
141. Horwitz EM, Gordon PL, Koo WK, et al. Isolated allogeneic bone marrow-derived mesenchymal cells engraft and stimulate growth in children with osteogenesis imperfecta: implications for cell therapy of bone. Proc Natl Acad Sci USA. 2002 99 : 8932 8937.
142. Di Nicola M, Carlo-Stella C, Magni M, et al. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood. 2002 99 : 3838 3843.
143. Romieu-Mourez R, Francois M, Boivin MN, et al. Regulation of MHC class II expression and antigen processing in murine and human mesenchymal stromal cells by IFN-gamma, TGF-beta, and cell density. J Immunol. 2007 179 : 1549 1558.
144. Morelli AE, Thomson AW. Dendritic cells: regulators of alloimmunity and opportunities for tolerance induction. Immunol Rev. 2003 196 : 125 146.
145. Jiang XX, Zhang Y, Liu B, et al. Human mesenchymal stem cells inhibit differentiation and function of monocyte-derived dendritic cells. Blood. 2005 105 : 4120 4126.
146. Brusko TM, Putnam AL, Bluestone JA. Human regulatory T cells: role in autoimmune disease and therapeutic opportunities. Immunol Rev. 2008 223 : 371 390.
147. Degauque N, Mariat C, Kenny J, et al. Immunostimulatory Tim-1-specific antibody deprograms Tregs and prevents transplant tolerance in mice. J Clin Invest. 2008 118 : 735 741.
148. Hince M, Sakkal S, Vlahos K, et al. The role of sex steroids and gonadectomy in the control of thymic involution. Cell Immunol. 2008 252 : 122 138.
149. Ildstad ST, Sachs DH. Reconstitution with syngeneic plus allogeneic or xenogeneic bone marrow leads to specific acceptance of allografts or xenografts. Nature. 1984 307 : 168 170.
150. Ildstad ST, Wren SM, Bluestone JA, et al. Characterization of mixed allogeneic chimeras. Immunocompetence, in vitro reactivity, and genetic specificity of tolerance. J Exp Med. 1985 162 : 231 244.
151. Kawai T, Cosimi AB, Spitzer TR, et al. HLA-mismatched renal transplantation without maintenance immunosuppression. N Engl J Med. 2008 358 : 353 361.
152. Alpdogan O, Schmaltz C, Muriglan SJ, et al. Administration of interleukin-7 after allogeneic bone marrow transplantation improves immune reconstitution without aggravating graft-versus-host disease. Blood. 2001 98 : 2256 2265.
153. Wils EJ, Braakman E, Verjans GM, et al. Flt3 ligand expands lymphoid progenitors prior to recovery of thymopoiesis and accelerates T cell reconstitution after bone marrow transplantation. J Immunol. 2007 178 : 3551 3557.
154. Sutherland JS, Goldberg GL, Hammett MV, et al. Activation of thymic regeneration in mice and humans following androgen blockade. J Immunol. 2005 175 : 2741 2753.
155. Heng TS, Goldberg GL, Gray DH, et al. Effects of castration on thymocyte development in two different models of thymic involution. J Immunol. 2005 175 : 2982 2993.
156. Fandrich F, Dresske B, Bader M, et al. Embryonic stem cells share immune-privileged features relevant for tolerance induction. J Mol Med. 2002 80 : 343 350.
157. Koch KS, Son KH, Maehr R, et al. Immune-privileged embryonic Swiss mouse STO and STO cell-derived progenitor cells: major histocompatibility complex and cell differentiation antigen expression patterns resemble those of human embryonic stem cell lines. Immunology. 2006 119 : 98 115.
158. Priddle H, Jones DR, Burridge PW, et al. Hematopoiesis from human embryonic stem cells: overcoming the immune barrier in stem cell therapies. Stem Cells. 2006 24 : 815 824.
159. Robertson NJ, Brook FA, Gardner RL, et al. Embryonic stem cell-derived tissues are immunogenic but their inherent immune privilege promotes the induction of tolerance. Proc Natl Acad Sci USA. 2007 104 : 20920 20925.
160. Wu DC, Boyd AS, Wood KJ. Embryonic stem cells and their differentiated derivatives have a fragile immune privilege but still represent novel targets of immune attack. Stem Cells. 2008 26 : 1939 1950.
161. Ilancheran S, Michalska A, Peh G, et al. Stem cells derived from human fetal membranes display multilineage differentiation potential. Biol Reprod. 2007 77 : 577 588.
162. Troyer DL, Weiss ML. Wharton's jelly-derived cells are a primitive stromal cell population. Stem Cells. 2008 26 : 591 599.
163. Weiss ML, Anderson C, Medicetty S, et al. Immune properties of human umbilical cord Wharton's jelly-derived cells. Stem Cells. 2008 26 : 2865 2874.
164. Weiss ML, Medicetty S, Bledsoe AR, et al. Human umbilical cord matrix stem cells: preliminary characterization and effect of transplantation in a rodent model of Parkinson's disease. Stem Cells. 2006 24 : 781 792.
165. Montjovent MO, Bocelli-Tyndall C, Scaletta C, et al. In vitro characterization of immune-related properties of human fetal bone cells for potential tissue engineering applications. Tissue Eng A. 2009 15 : 1523 1532.
166. Morrow CM, Hostetler CE, Griswold MD, et al. ETV5 is required for continuous spermatogenesis in adult mice and may mediate blood testes barrier function and testicular immune privilege. Ann N Y Acad Sci. 2007 1120 : 144 151.
167. Paus R, Arck P, Tiede S. (Neuro-) endocrinology of epithelial hair follicle stem cells. Mol Cell Endocrinol. 2008 288 : 38 51.
168. Thomson JA, Odorico JS. Human embryonic stem cell and embryonic germ cell lines. Trends Biotechnol. 2000 18 : 53 7.
169. Amit M, Itskovitz-Eldor J. Derivation and spontaneous differentiation of human embryonic stem cells. J Anat. 2002 200 : 225 232. (Pubitemid 34467314)
170. Kastenberg ZJ, Odorico JS. Alternative sources of pluripotency: science, ethics, and stem cells. Transplant Rev. 2008 22 : 215 222.
171. Amit M, Shariki C, Margulets V, et al. Feeder layer- and serum-free culture of human embryonic stem cells. Biol Reprod. 2004 70 : 837 845. (Pubitemid 38233724)
172. Xu C, Inokuma MS, Denham J, et al. Feeder-free growth of undifferentiated human embryonic stem cells. Nat Biotechnol. 2001 19 : 971 974. (Pubitemid 32947578)
173. Klimanskaya I, Chung Y, Meisner L, et al. Human embryonic stem cells derived without feeder cells. Lancet. 2005 365 : 1636 1641. (Pubitemid 40693413)
174. Allegrucci C, Wu YZ, Thurston A, et al. Restriction landmark genome scanning identifies culture-induced DNA methylation instability in the human embryonic stem cell epigenome. Hum Mol Genet. 2007 16 : 1253 1268.
175. Condic ML, Rao M. Regulatory issues for personalized pluripotent cells. Stem Cells. 2008 26 : 2753 2758.
176. Le Blanc K, Samuelsson H, Gustafsson B, et al. Transplantation of mesenchymal stem cells to enhance engraftment of hematopoietic stem cells. Leukemia. 2007 21 : 1733 1738.
177. Roy NS, Nakano T, Keyoung HM, et al. Telomerase immortalization of neuronally restricted progenitor cells derived from the human fetal spinal cord. Nat Biotechnol. 2004 22 : 297 305.
178. Smith SB, Gasa R, Watada H, et al. Neurogenin3 and hepatic nuclear factor 1 cooperate in activating pancreatic expression of Pax4. J Biol Chem. 2003 278 : 38254 38259.
179. Vassilopoulos G, Wang PR, Russell DW. Transplanted bone marrow regenerates liver by cell fusion. Nature. 2003 422 : 901 904.
180. Rizzino A. A challenge for regenerative medicine: proper genetic programming, not cellular mimicry. Dev Dyn. 2007 236 : 3199 3207.
181. Clarke DL, Johansson CB, Wilbertz J, et al. Generalized potential of adult neural stem cells. Science. 2000 288 : 1660 1663.
182. D'Amour KA, Gage FH. Genetic and functional differences between multipotent neural and pluripotent embryonic stem cells. Proc Natl Acad Sci USA. 2003 100 : 11866 11872.