In-utero stem cell transplantation: Clinical use and therapeutic potential

Minerva Ginecologica

Volumn 63, Issue 4, 2011, Pages 387-398

  De Santis, M ^a   De Luca, C ^a   Mappa, I ^a   Cesari, E ^a   Quattrocchi, T ^a   Spagnuolo, T ^a   Visconti, D ^a   Noia, G ^a   Caruso, A ^a  

^a CATHOLIC UNIVERSITY   (Italy)

Author keywords

Fetal tissue transplantation; Hematopoietic stem cells; Stem cells

Indexed keywords

LENTIVIRUS VECTOR;

ADENO ASSOCIATED VIRUS; ADULT STEM CELL; ANIMAL MODEL; BLASTOCYST; CASE REPORT; CELL DIFFERENTIATION; CELL RENEWAL; CRIGLER NAJAR; CYSTIC FIBROSIS; DUCHENNE MUSCULAR DYSTROPHY; EMBRYONIC STEM CELL; ENDOTHELIUM CELL; ENGRAFTMENT; EPITHELIUM CELL; FETUS; GENE THERAPY; GENETIC DISORDER; GERM LINE GENE THERAPY; GLOBOID CELL LEUKODYSTROPHY; GLYCOGEN STORAGE DISEASE TYPE 2; GRAFT VERSUS HOST REACTION; HEART MUSCLE CELL; HEMATOPOIETIC STEM CELL; HEMOGLOBINOPATHY; HEMOPHILIA A; HLA SYSTEM; HUMAN; HUMAN AMNIOTIC MESENCHYMAL STROMAL CELL; HUMAN CHORIONIC MESENCHYMAL STROMAL CELL; HURLER SYNDROME; IMMUNE DEFICIENCY; IMMUNE RESPONSE; IMMUNOSUPPRESSIVE TREATMENT; IN UTERO STEM CELL TRANSPLANTATION; IN VITRO STUDY; LEBER CONGENITAL AMAUROSIS; MEDICAL ETHICS; MESENCHYMAL STEM CELL; METABOLIC DISORDER; METACHROMATIC LEUKODYSTROPHY; MUCOPOLYSACCHARIDOSIS TYPE 7; MYELOABLATIVE CONDITIONING; NERVE CELL; NIEMANN PICK DISEASE; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; OSTEOGENESIS IMPERFECTA; OUTCOME ASSESSMENT; PANCREAS; PLACENTA; PRENATAL DIAGNOSIS; REVIEW; RHESUS ISOIMMUNIZATION; RISK BENEFIT ANALYSIS; RISK REDUCTION; SAFETY; SKELETAL MUSCLE; STEM CELL; STORAGE DISEASE; T LYMPHOCYTE; TOTIPOTENT STEM CELL; UMBILICAL CORD BLOOD; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY;

ADULT STEM CELLS; EMBRYONIC STEM CELLS; FEMALE; FETAL DISEASES; FETUS; GENE THERAPY; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; MESENCHYMAL STEM CELL TRANSPLANTATION; PREGNANCY; STEM CELL TRANSPLANTATION;

EID: 80054749120     PISSN: 00264784     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (102)

1. Wobus AM, Boheler KR. Embryonic stem cells: prospects for developmental biology and cell therapy. Physiol Rev 2005;85:635-78. (Pubitemid 40404638)
2. Weissman IL, Shizuru JA. The origins of the identification and isolation of hematopoietic stem cells, and their capability to induce donor-specific transplantation tolerance and treat autoimmune diseases. Blood 2008;112:3543-53.
3. Christensen JL, Wright DE, Wagers AJ, Weissman IL. Circulation and Chemotaxis of fetal hematopoietic stem cells. PLoS Biol 2004;2:E75.
4. Haspel RL, Miller KB. Hematopoietic stem cells: source matters. Curr Stem Cell Res Ther 2008;3:229-36.
5. Chen LB, Jiang XB. Differentiation of rat marrow mesenchymal stem cells into pancreatic islet beta-cells. World J Gastroenterol 2004;10:3016-20.
6. Barrilleaux B, Phinney DG, Prockop DJ, O'Connor KC. Review: ex vivo engineering of living tissues with adult stem cells. Tissue Eng 2006;12:3007-19. (Pubitemid 44846407)
7. De Coppi P, Barstch G, Atala A. Isolation of amniotic stem cell lines with potential for therapy. Nature Biothecnology 2007;25:100-6. (Pubitemid 46087908)
8. Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, Zucker JP et al. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 2005;122:947-56. (Pubitemid 41345211)
9. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS et al. Embryonic stem cell lines derived from human blastocysts. Science 1998;282:1145-7. (Pubitemid 28516247)
10. Adewumi O, Aflatoonian B, Ahrlund-Richter L, Amit M, Andrews PW, Beighton G et al. Characterization of human embryonic stem cell lines by the International Stem Cell Initiative. Nat Biotechnol 2007;25:803-16. (Pubitemid 47052190)
11. Gardner RL. Stem cells: potency, plasticity and public perception. J Anat 2002;200:277-82. (Pubitemid 34467320)
12. Jiang Y, Jahagirdar BN, Reinhardt RL, Schwartz RE, Keene CD, Ortiz-Gonzalez XR et al. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 2002;418:41-9. (Pubitemid 34742565)
13. Gavrilov S, Papaioannou VE, Landry DW. Alternative strategies for the derivation of human embryonic stem cell lines and the role of dead embryos. Curr Stem Cell Res Ther 2009;4:81-6.
14. Greely HT, Hamm T, Johnson R, Price CR, Weingarten R, Raffin T. The ethical use of human fetal tissue in medicine. Stanford University Medical Center Committee on Ethics. N Engl J Med 1989;320:1093-6.
15. Zipori D. The stem state: plasticity is essential, whereas self-renewal and hierarchy are optional. Stem Cells 2005;23:719-26. (Pubitemid 40791787)
16. Parolini O, Alviano F, Bagnara GP, Bilic G, Bühring HJ, Evangelista M et al. Concise review: isolation and characterization of cells from human term placenta: outcome of the first international Workshop on Placenta Derived Stem Cells. Stem Cells 2008;26:300-11.
17. Delorme B, Chateauvieux S, Charbord P. The concept of mesenchymal stem cells. Regen Med 2006;1:497-509.
18. Miki T, Lehmann T, Cai H, Stolz DB, Strom SC. Stem cell characteristics of amniotic epithelial cells. Stem Cells 2005;23:1549-59. (Pubitemid 41741004)
19. Soncini M, Vertua E, Gibelli L, Zorzi F, Denegri M, Albertini A et al. Isolation and characterization of mesenchymal cells from human fetal membranes. J Tissue Eng Regen Med 2007;1:296-305.
20. Troyer DL, Weiss ML Wharton's jelly-derived cells are a primitive stromal cell population. Stem Cells 2008;26:591-9.
21. Can A, Karahuseyinoglu S. Concise review: human umbilical cord stroma with regard to the source of fetus-derived stem cells. Stem Cells 2007;25:2886-95. (Pubitemid 350127873)
22. Siegel N, Rosner M, Hanneder M, Valli A, Hengstschläger M. Stem cells in amniotic fluid as new tools to study human genetic diseases Stem Cell Rev 2007;3:256-64. (Pubitemid 351526202)
23. Gluckman E, Devergie A, Thierry D, Esperou-Bourdeau H, Traineau R, Gerrota J et al. Clinical applications of stem cell transfusion from cord blood and rationale for cord blood banking. Bone Marrow Transplant 1992;9(Suppl 1):114-7.
24. Broxmeyer HE, Gluckman E, Auerbach A, Douglas GW, Friedman H, Cooper S et al. Human umbilical cord blood: a clinically useful source of transplantable hematopoietic stem/progenitor cells. Int J Cell Cloning 1990;8(Suppl 1):76-89; discussion 89-91.
25. Pahwa RN, Fleischer A, Than S, Good RA. Successful hematopoietic reconstitution with transplantation of erythrocyte-depleted allogeneic human umbilical cord blood cells in a child with leukemia. Proc Natl Acad Sci U S A 1994;91:4485-8. (Pubitemid 24143458)
26. Solves P, Mirabet V, Perales A, Carbonell-Uberos F, Roig R. Banking strategies for improving the hematopoietic stem cell content of umbilical cord blood units for transplantation. Curr Stem Cell Res Ther 2008;3:79-84. (Pubitemid 352024853)
27. Bieback K, Klüter H. Mesenchymal stromal cells from umbilical cord blood. Curr Stem Cell Res Ther 2007;2:310-23.
28. Erices AA, Allers CI, Conget PA, Rojas CV, Minguell JJ.Human cord blood-derived mesenchymal stem cells home and survive in the marrow of immunodeficient mice after systemic infusion. Cell Transplant 2003;12:555-61. (Pubitemid 37204412)
29. Troeger C, Surbek D, Schöberlein A, Schalt S, Dudler L, Hahn S et al. In utero haematopoietic stem cell transplantation. Experiences in mice, sheep and humans. Swiss Med Wkly 2006;137(Suppl 155):14S-9S.
30. Surbek DV, Holzgreve W, Nicolaides KH. Haematopoietic stem cell transplantation and gene therapy in the fetus: ready for clinical use? Hum Reprod Update 2001;7:85-91. (Pubitemid 32111974)
31. Stites DP, Carr MC, Fudenberg HH. Ontogeny of cellular immunity in the human fetus: development of responses to phytohemagglutinin and to allogeneic cells. Cell Immunol 1974;11:257-71.
32. Rayfield LS, Brent L, Rodeck CH. Development of cell-mediated lympholysis in human foetal blood lymphocytes. Clin Exp Immunol 1980;42:561-70. (Pubitemid 11247479)
33. Thilaganathan B, Mansur CA, Morgan G, Nicolaides KH. Fetal T-lymphocyte subpopulations in normal pregnancies. Fetal Diagn Ther 1992;7:53-61.
34. Takahama Y. Journey through the thymus: stromal guides for T-cell development and selection. Nat Rev Immunol 2006;6:127-35. (Pubitemid 43361588)
35. Flake AW, Zanjani ED. In-utero hematopoietic stem cell transplantation: Ontogenic opportunities and biologic barriers. Blood 1999;94:2179-91. (Pubitemid 29467663)
36. a G, Pierelli L, Bonanno G, Monego G, Perillo A, Rutella S et al. A novel route of transplantation of human cord blood stem cells in preimmune fetal sheep: the intracelomic cavity. Stem Cells 2003;21:638-46.
37. Noia G, Pierelli L, Bonanno G, Monego G, Perillo A, Rutella S et al. The intracoelomic route: a new approach for in utero human cord blood stem cell transplantation. Fetal Diagn Ther 2004;19:13-22. (Pubitemid 37500546)
38. Noia G, Ligato MS, Cesari E, Visconti D, Fortunato G, Tintoni M et al. Source of cell injected is a critical factors for short and long engraftment in xenotransplantation. Cell Prolif 2008;41(Suppl 1):41-50. (Pubitemid 350295850)
39. Westgren M. In utero stem cell transplantation. Semin Reprod Med 2006;24:348-57. (Pubitemid 44877578)
40. Muench MO, Bárcena A. Stem cell transplantation in the fetus. Cancer Control 2004;11:105-18. (Pubitemid 38596195)
41. Davies J. Clinicopathological conference. A case of haemolytic disease with congenital rubella demonstrated at the Roya Postgraduate Medical School. Br Med J 1967;2:819-22.
42. Touraine JL, Raudrant D, Royo C, Rebaud A, Roncarolo MG, Souillet G et al. In-utero transplantation of stem ceils in bare lymphocyte syndrome. Lancet 1989;1:1382. (Pubitemid 19151967)
43. Flake AW, Roncarolo MG, Puck JM, Almeida-Porada G, Evans MI, Johnson MP et al. Treatment of X linked severe combined immunodeficiency by in utero trans-plantation of paternal bone marrow. N Engl J Med 1996;335:1806-10. (Pubitemid 26412399)
44. Wengler GS, Lanfranchi A, Frusca T, Verardi R, Neva A, Brugnoni D et al. In-utero transplantation of parental CD34 haematopoietic progenitor cells in a patient with X-linked severe combined immunodeficiency (SCIDXI). Lancet 1996;348:1484-7. (Pubitemid 26400245)
45. Lanfranchi A, Neva A, Tettoni K, Veradi R, Mazzolari E, Wengler G et al. In utero transplantations of parental CD34+ cells in three patients affected by primary immunodeficiencies. Bone Marrow Transplant 1998;21:S127.
46. Westgren M, Ringdén O, Bartmann P, Bui TH, Lindton B, Mattsson J et al. Prenatal T-cell reconstitution after in utero transplantation with fetal liver cells in a patient with X-linked severe combined immunodeficiency. Am J Obstet Gynecol 2002;187:475-82. (Pubitemid 34925591)
47. Pirovano S, Notarangelo LD, Malacarne F, Mazzolari E, Porta F, Lanfranchi A et al. Reconstitution of T-cell compartment after in utero stem cell transplantation: analysis of T-cell repertoire and thymic output. Haematologica 2004;89:450-61. (Pubitemid 38798550)
48. Porta F, Mazzolari E, Zucca S, Schumacher F, Lanfranchi A, Tettoni K et al. Prenatal transplant in a fetus affected by omenn syndrome. Bone Marrow Transplant 2000;25:S43-4.
49. Hayward A, Ambruso D, Battaglia F, Donlon T, Eddelman K, Giller R et al. Microchimerism and tolerance following intrauterine transplantation and transfusion for a-thalassemia-1. Fetal Diagnosis and Therapy 1998;13:8-14. (Pubitemid 28171755)
50. Diukman R, Golbus MS. In utero stem cell therapy. J Reprod Med 1992;37:515.
51. Bambach BJ, Moser HW, Blakemore K, Corson VL, Griffin CA, Noga SJ et al. Engraftment following in utero bone marrow transplantation for globoid cell leukodystrophy. Bone Marrow Transplant 1997;19:399-402. (Pubitemid 27096076)
52. Touraine JL, Raudrant D, Golfier F, Rebaud A, Sembeil R, Roncarolo MG et al. Reappraisal of in utero stem cell transplantation based on long-term results. Fetal Diagn Ther 2004;19:305-12. (Pubitemid 38822748)
53. Flake AW, Zanjani ED. In Utero Hematopoietic Stem Cell Transplantation: Ontogenic Opportunities and biologic barrier. Blood 1999;94:2179-91. (Pubitemid 29467663)
54. Muench MO, Rae J, Bárcena A, Leemhuis T, Farrell J, Humeau L et al. Transplantation of a fetus with paternal Thy-1+ CD34+ cells for chronic granulomatous disease. Bone Marrow Transplantion 2001;27:355-64. (Pubitemid 32201343)
55. Westgren M, Ringden O, Eik-Nes S, Ek S, Anvret M, Brubakk AM et al. Lack of evidence of permanent engraftment after in utero fetal stem cell transplantation in congenital hemoglobinopathies. Transplantation 1996;61:1176-9. (Pubitemid 26134766)
56. Touraine JL, Raudrant D, Royo, Rebaud A, Roncarolo MG, Souillet G et al. In utero transplantation of hemopoietic stem cells in humans. Transplant Proc 1991;23(1 Pt 2):1706-8.
57. Slavin S, Naparstek E, Ziegler M, Lewin A. Clinical application of intrauterine bone marrow transplantation for treatment of genetic diseases - feasibility studies. Bone Marrow Transplant 1992;9:189-90.
58. Cowan MJ, Golbus M. In utero hematopoietic stem cell transplants for inherited diseases. Am J Pediatr Hematol Oncol 1994;16:35-42. (Pubitemid 24046456)
59. Orlandi F, Giambona A, Messana F, Marino M, Abate I, Calzolari R et al. Evidence of induced non-tolerance in HLA-identical twins with hemoglobinopathy after in utero fetal transplantation. Bone Marrow Transplant 1996;18:637-9. (Pubitemid 26316016)
60. Peschle C, Contu L, Melis G. In utero transplantation of purified stem cells from an HLA identical sibling into a betathalassemia embryo. Second International Meeting for In Utero Stem Cell Transplantation and Gene Therapy; 1997 September 1-3; Nottingham, England.
61. Monni G, Ibba RM, Zoppi MA, Floris M. In utero stem cell transplantation. Croat Med J 1998;39:220-3. (Pubitemid 28288563)
62. Shields LE, Lindton B, Andrews RG, Westgren MJ. Fetal hematopoietic stem cell transplantation: a challenge for the twenty-first century. Hematother Stem Cell Res 2002;11:617-31. (Pubitemid 34851793)
63. Renda MC, Daimiani G, Fecarotta E. In utero stem cell transplantation after a mild immunosuppression:evidence of paternal ABO cDNA in B -thalassemia affected fetus. Blood Transfus 2005;3:55-65.
64. Linch D, Rodeck C, Nicolaides K. Attempted bone marrow transplantation in a 17 week fetus. Lancet 1986;1:1382.
65. Thalaganthan B, Nicolaides K. Intrauterine bonemarrow transplantation at 12 weeks gestation. Lancet 1993;342:243. (Pubitemid 23214658)
66. Leung W, Blakemore K, Jones RJ, Moser HW, Mukherjee G, Griffin CA et al. A human-murine chimera model for in utero human hematopoietic stem cell transplantation. Biol Blood Marrow Transplant 1999;5:1-7.
67. FlakeAW, Zanjani ED. In utero hematopoietic stem cell transplantation. Astatus report. JAMA 1997;278:932.
68. O'Donoghue K, Chan J. Human fetal mesenchymal stem cells. Curr Stem Cell Res Ther 2006;1:371-86.
69. Wagner A, Shoeberlein A, Surbek D. Fetal gene therapy: opportunities and risks. Advanced Drug Delivery Reviews 2009;61:814-21.
70. Rauch F, Glorieux FH. Osteogenesis imperfecta. Lancet 2004;363:1377-85. (Pubitemid 38529880)
71. Horwitz EM, Prockop DJ, Fitzpatrick LA, Koo WW, Gordon PL, Neel M et al. Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta. Nat Med 1999;5:309-13. (Pubitemid 29124367)
72. Horwitz EM, Gordon PL, Koo WK, Marx JC, Neel MD, McNall RY 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 U S A 2002;99:8932-7. (Pubitemid 34693661)
73. Liechty KW, MacKenzie TC, Shaaban AF, Radu A, Moseley AM, Deans R et al. Human mesenchymal stem cells engraft and demonstrate sitespecific differentiation after in utero transplantation in sheep. Nat Med 2000;6:1282-6.
74. Mackenzie TC, Flake AW. Human mesenchymal stem cells persist, demonstrate site-specific multipotential differentiation, and are present in sites of wound healing and tissue regeneration after transplantation into fetal sheep. Blood Cells Mol Dis 2001;27:601-4. (Pubitemid 32757054)
75. Schoeberlein A, Holzgreve W, Dudler L, Hahn S, Surbek DV. Tissue-specific engraftment after in utero transplantation of allogeneic mesenchymal stem cells into sheep fetuses. Am J Obstet Gynecol 2005;192:1044-52. (Pubitemid 40487777)
76. Guillot PV, Abass O, Bassett JH, Shefelbine SJ, BouGharios G, Chan J et al. Intrauterine transplantation of human fetal mesenchymal stem cells from first-trimester blood repairs bone and reduces fractures in osteogenesis imperfecta mice. Blood 2008;111:1717-25. (Pubitemid 351213464)
77. Le Blanc K, Götherström C, Ringdén O, Hassan M, McMahon R, Horwitz E et al. Fetal mesenchymal stem-cell engraftment in bone after in utero transplantation in a patient with severe osteogenesis imperfecta. Transplantation 2005;79:1607-14. (Pubitemid 40847594)
78. Di Nicola M, Carlo-Stella C, Magni M, Milanesi M, Longoni PD, Matteucci P et al. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or non-specific mitogenic stimuli. Blood 2002;99:3838-43. (Pubitemid 34534559)
79. Gotherstrom C, Ringden O, Tammik C, Zetterberg E, Westgren M, Le Blanc K. Immunological properties of human fetal mesenchymal stem cells. Am J Obstet Gynecol 2004;190:239-45. (Pubitemid 38156354)
80. Gotherstrom C, Ringden O, Westgren M, Tammik L, Le Blanc K. Immunomodulatory effects of human foetal liver derived mesenchymal stem cells. Bone Marrow Transplant 2003;32:265-72. (Pubitemid 36927077)
81. Mackenzie TC, Shaaban AF, Radu A, Flake AW. Engraftment of bone marrow and fetal liver cells after in utero transplantation in MDX mice. J Pediatr Surg 2002;37:1058-64. (Pubitemid 34742845)
82. De Bari C, Dell'Accio F, Vandenabeele F, Vermeesch JR, Raymackers JM, Luyten FP. Skeletal muscle repair by adult human mesenchymal stem cells from synovial membrane. J Cell Biol 2003;160:909-18. (Pubitemid 36350845)
83. Senut MC, Gage FH. Prenatal gene therapy: can the technical hurdles be overcome? Mol Med Today 1999;5:152-6. (Pubitemid 29279825)
84. Verma IM, Somia N. Gene therapy - promises, problems and prospects. Nature 1997;389:239-42. (Pubitemid 27406627)
85. Roybal JL, Santore MT, Flake AW. Stem cell and genetic therapies for the fetus. Seminars in Fetal and Neonatal Medicine 2010;15:46-51.
86. Jimenez DF, Lee CI, O'Shea CE, Kohn DB, Tarantal AF. HIV-1-derived lentiviral vectors and fetal route of administration on transgene biodistribution and expression in rhesus monkeys. Gene Ther 2005;12:821-30. (Pubitemid 40753974)
87. Lee CC, Jimenez DF, Kohn DB, Tarantal AF. Fetal gene transfer using lentiviral vectors and the potential for germ cell transduction in rhesus monkeys (Macaca mulatta). Hum Gene Ther 2005;16:417-25. (Pubitemid 40647139)
88. Seppen J, van der Rijt R, Looije N, van Til NP, Lamers WH, Oude Elferink RP. Long-term correction of bilirubin UDPglucuronyltransferase deficiency in rats by in utero lentiviral gene transfer. Mol Ther 2003;83:593-9. (Pubitemid 37321688)
89. Tsukamoto M, Ochiya T, Yoshida S, Sugimura T, Terada M. Gene transfer and expression in progeny after intravenous DNA injection into pregnant mice. Nat Genet 1995;9:243-8.
90. Billings PR. In utero gene therapy: the case against. Nat Med 1999;5:255-6. (Pubitemid 29124350)
91. King D, Shakespeare T, Nicholson R, Clarke A, McLean S. Risks inherent in fetal gene therapy. Nature 1999;397:383.
92. Han J, Sidhu KS. Current concepts in reprogramming somatic cells to pluripotent state. Curr Stem Cell Res Ther 2008;3:66-74. (Pubitemid 352024869)
93. Wilmut I, Schnieke A E, McWhir, J, Kind AJ, Campbell KH. Viable offspring derived from fetal and adult mammalian cells. Nature 1997;385:810-3. Erratum in: Nature 1997;386(6621):200. (Pubitemid 27106068)
94. Tada M, Takahama Y, Abe K, Nakatsuji N, Tada, T. Nuclear reprogramming of somatic cells by in vitro hybridization with ES cells. Curr Biol 2001;11:1553-8. (Pubitemid 32931020)
95. Cowan CA, Atienza J, Melton DA, Eggan K. Nuclear reprogramming of somatic cells after fusion with human embryonic stem cells. Science 2005;309(5739):1369-7.
96. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006;126:663-76. (Pubitemid 44233629)
97. Wernig M, Meissner A, Foreman R. In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature 2007;448:318-24. (Pubitemid 47080337)
98. Okita K, Ichisaka T, Yamanaka S. Generation of germline-competent induced pluripotent stem cells. Nature 2007;448:313-7. (Pubitemid 47080336)
99. Maherali N, Sridharan R, Xie W, Utikal J, Eminli S, Arnold K et al. Directly reprogrammed fibroblasts show global epigenetic remodeling and widespread tissue contribution. Cell Stem Cell 2007;1:55-70.
100. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S et al. Induced Pluripotent Stem Cell Lines Derived from Human Somatic Cells Science. Science 2007;318:1917-20.
101. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007;131:861-72. (Pubitemid 350138099)
102. Park IH, Zhao R, West JA, Yabuuchi A, Huo H, Ince TA et al. Reprogramming of human somatic cells to pluripotency with defined factors. Nature 2008;451:141-6.