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Chapter 20.2 - Fetal stem cell transplantation

Clinical potential

from Section 2 - Fetal disease

Published online by Cambridge University Press:  05 February 2013

Mark D. Kilby
Affiliation:
Department of Fetal Medicine, University of Birmingham
Anthony Johnson
Affiliation:
Baylor College of Medicine, Texas
Dick Oepkes
Affiliation:
Department of Obstetrics, Leiden University Medical Center
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Summary

Introduction

Over the past decades fetal medicine with fetal therapy has evolved as a new field within obstetrics. Different treatment strategies have been explored and one of those is fetal stem cell transplantation. The rational for in-utero stem cell transplantation is based on the assumptions that treatment before birth is preferable because the target disease is either lethal for the fetus or will result in early childhood morbidity, making postnatal therapy less efficacious. In-utero stem cell transplantation should potentially represent a major step forward in the management of patients with congenital, hematological, metabolic, and immunological disorders. Traditionally the early first and second trimester fetus has been described as preimmune, i.e., incapable of mounting an adaptive immune response to allogeneic cells or pathogens. The concept of in-utero transplantations (IUTs) aims to take advantage of the naïve immunological system, and consequently transplantations could potentially be carried out across histoincompatibility barriers and with no need for immunomodulation or cytoablation.

The human fetus was subjected to treatment attempts with stem cell transplantation in 1989 when Touraine et al. published their first case [1] of IUT in a human fetus affected by bare lymphocyte syndrome. Since then we know of several X-severe combined immunodeficiency disease (SCID) cases treated in utero with stem cells [2–4]. All these children survived and were chimeric at birth.

Type
Chapter
Information
Fetal Therapy
Scientific Basis and Critical Appraisal of Clinical Benefits
, pp. 397 - 406
Publisher: Cambridge University Press
Print publication year: 2012

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References

Touraine, JL, Raudrant, D, Royo, C, et al. In-utero transplantation of stem cells in bare lymphocyte syndrome. Lancet 1989;1:1382.Google Scholar
Flake, AW, Roncarolo, MG, Puck, JM, et al. Treatment of x-linked severe combined immunodeficiency by in utero transplantation of paternal bone marrow. N Engl J Med 1996;335:1806–10.Google Scholar
Lanfranchi, A, Neva, A, Tettoni, K, et al. In utero transplantation (iut) of parental cd34+ cells in patient affected by primary immunodeficiencies. Bone Marrow Transplant 1998;21:S127 Google Scholar
Westgren, M, Ringden, O, Bartmann, P, 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.Google Scholar
Flake, AW, Zanjani, ED. In utero hematopoietic stem cell transplantation: ontogenic opportunities and biologic barriers. Blood 1999;94:2179–91.Google Scholar
Westgren, M, Ringden, O, Eik-Nes, S, et al. Lack of evidence of permanent engraftment after in utero fetal stem cell transplantation in congenital hemoglobinopathies. Transplantation 1996;61:1176–9.Google Scholar
Blazar, BR, Taylor, PA, Vallera, DA. In utero transfer of adult bone marrow cells into recipients with severe combined immunodeficiency disorder yields lymphoid progeny with T- and B-cell functional capabilities. Blood 1995;86:4353–66.Google Scholar
Fleischman, RA, Mintz, B. Prevention of genetic anemias in mice by microinjection of normal hematopoietic stem cells into the fetal placenta. Proc Natl Acad Sci U S A 1979;76:5736–40.Google Scholar
Mintz, B, Anthony, K, Litwin, S. Monoclonal derivation of mouse myeloid and lymphoid lineages from totipotent hematopoietic stem cells experimentally engrafted in fetal hosts. Proc Natl Acad Sci U S A 1984;81:7835–9.Google Scholar
Carrier, E, Lee, TH, Busch, MP, et al. Induction of tolerance in nondefective mice after in utero transplantation of major histocompatibility complex-mismatched fetal hematopoietic stem cells. Blood 1995;86:4681–90.Google Scholar
Hajdu, K, Tanigawara, S, McLean, LK, et al. In utero allogeneic hematopoietic stem cell transplantation to induce tolerance. Fetal Diagn Ther 1996;11:241–8.Google Scholar
Kim, HB, Shaaban, AF, Yang, EY, et al. Microchimerism and tolerance after in utero bone marrow transplantation in mice. J Surg Res 1998;77:1–5.Google Scholar
Brecher, G, Tjio, JH, Haley, JE, et al. Transplantation of murine bone marrow without prior host irradiation. Blood Cells 1979;5:237–46.Google Scholar
Slavin, S, Nagler, A, Aker, M, et al. Non-myeloablative stem cell transplantation and donor lymphocyte infusion for the treatment of cancer and life-threatening non-malignant disorders. Rev Clin Exp Hematol 2001;5:135–46.Google Scholar
Stewart, FM, Crittenden, RB, Lowry, PA, et al. Long-term engraftment of normal and post-5-fluorouracil murine marrow into normal nonmyeloablated mice. Blood 1993;81:2566–71.Google Scholar
Sykes, M, Preffer, F, McAfee, S, et al. Mixed lymphohaemopoietic chimerism and graft-versus-lymphoma effects after non-myeloablative therapy and HLA-mismatched bone-marrow transplantation. Lancet 1999;353:1755–9.Google Scholar
Merianos, DJ, Tiblad, E, Santore, MT, et al. Maternal alloantibodies induce a postnatal immune response that limits engraftment following in utero hematopoietic cell transplantation in mice. J Clin Invest 2009;9:2590–600.Google Scholar
Nijagal, A, Wegorzewska, M, Jarvis, E, et al. Maternal T cells limit engraftment after in utero hematopoietic cell transplantation in mice. J Clin Invest 2011;2:582–92.Google Scholar
Flake, AW, Harrison, MR, Adzick, NS, et al. Transplantation of fetal hematopoietic stem cells in utero: the creation of hematopoietic chimeras. Science 1986;233:776–8.Google Scholar
Zanjani, ED, Ascensao, JL, Flake, AW, et al. The fetus as an optimal donor and recipient of hemopoietic stem cells. Bone Marrow Transplant 1992;10(Suppl 1):107–14.Google Scholar
Zanjani, ED, Ascensao, JL, Tavassoli, M. Liver-derived fetal hematopoietic stem cells selectively and preferentially home to the fetal bone marrow. Blood 1993;81:399–404.Google Scholar
Crombleholme, TM, Harrison, MR, Zanjani, ED. In utero transplantation of hematopoietic stem cells in sheep: the role of T-cells in engraftment and graft-versus-host disease. J Pediatr Surg 1990;25:885–92.Google Scholar
Zanjani, ED, Almeida-Porada, G, Ascensao, JL, et al. Transplantation of hematopoietic stem cells in utero. Stem Cells 1997;15(Suppl 1):79–92; discussion 93.Google Scholar
Hedrick, MH, Rice, HE, MacGillivray, TE, et al. Hematopoietic chimerism achieved by in utero hematopoietic stem cell injection does not induce donor-specific tolerance for renal allografts in sheep. Transplantation 1994;58:110–11.Google Scholar
Flake, AW, Hendrick, MH, Rice, HE, et al. Enhancement of human hematopoiesis by masT-cell growth factor in human-sheep chimeras created by the in utero transplantation of human fetal hematopoietic cells. Exp Hematol 1995;23:252–7.Google Scholar
Zanjani, ED, Flake, AW, Rice, H, et al. Long-term repopulating ability of xenogeneic transplanted human fetal liver hematopoietic stem cells in sheep. J Clin Invest 1994;93:1051–5.Google Scholar
Almeida-Porada, G, Flake, AW, Glimp, HA, et al. Cotransplantation of stroma results in enhancement of engraftment and early expression of donor hematopoietic stem cells in utero. Exp Hematol 1999;27:1569–75.Google Scholar
Almeida-Porada, G, Porada, CD, Tran, N, et al. Cotransplantation of human stromal cell progenitors into preimmune fetal sheep results in early appearance of human donor cells in circulation and boosts cell levels in bone marrow at later time points after transplantation. Blood 2000;95:3620–7.Google Scholar
Liubas, K. Hematopoietic stem and progenitorcells and potentials for application infetal cell replacement therapy. Thesis, University of Lund, 2009.
Blakemore, K, Hattenburg, C, Stetten, G, et al. In utero hematopoietic stem cell transplantation with haploidentical donor adult bone marrow in a canine model. Am J Obstet Gynecol 2004;190:960–73.Google Scholar
Harrison, MR, Slotnick, RN, Crombleholme, TM, et al. In-utero transplantation of fetal liver haemopoietic stem cells in monkeys. Lancet 1989;2:1425–7.Google Scholar
Brent, L, Linch, DC, Rodeck, CH, et al. On the feasibility of inducing tolerance in man: a study in the cynomolgus monkey. Immunol Lett 1989;21:55–61.Google Scholar
Roodman, GD, Kuehl, TJ, Vandeberg, JL, et al. In utero bone marrow transplantation of fetal baboons with mismatched adult baboon marrow. Blood Cells 1991;17:367–75.Google Scholar
Cowan, MJ, Tarantal, AF, Capper, J, et al. Long-term engraftment following in utero T-cell-depleted parental marrow transplantation into fetal rhesus monkeys. Bone Marrow Transplant 1996;17:1157–65.Google Scholar
Shields, LE, Gaur, L, Delio, P, et al. Fetal immune suppression as adjunctive therapy for in utero hematopoietic stem cell transplantation in nonhuman primates. Stem Cells 2004;22:759–69.Google Scholar
Shields, LE, Gaur, LK, Gough, M, et al. In utero hematopoietic stem cell transplantation in nonhuman primates: the role of T-cells. Stem Cells 2003;21:304–14.Google Scholar
Guillot, PV, Abass, O, Bassett, JH, et al. In utero 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.Google Scholar
Vanleene, M, Saldanha, Z, Cloyd, KL, et al. Transplantation of human fetal blood stem cells in the osteogenesis imperfecta mouse leads to improvement in multiscale tissue properties. Blood 2011;117(3):1053–60.Google Scholar
Panaroni, C, Gioia, R, Lupi, A, et al. In utero transplantation of adult bone marrow decreases perinatal lethality and rescues the bone phenotype in the knockin murine model for classical, dominant osteogenesis imperfecta. Blood 2009;114(2):459–68.Google Scholar
Chan, J, Waddington, SN, O’Donoghue, K, Kurata, H, Guillot, PV, Gotherstrom, C, Themis, M, Morgan, JE, Fisk, NM. Widespread distribution and muscle differentiation of human fetal mesenchymal stem cells after in utero transplantation in dystrophic mdx mouse. Stem Cells 2007;25:875–84.Google Scholar
Mackenzie, TC, Shaaban, AF, Radu, A, et al. Engraftment of bone marrow and fetal liver cells after in utero transplantation in MDX mice. J Pediatr Surg 2002;37(7):1058–64.Google Scholar
Guillot, PV, Cook, HT, Pusey, CD, et al. Transplantation of human fetal mesenchymal stem cells improves glomerulopathy in a collagen type I alpha 2-deficient mouse. J Pathol 2008;214:627–63.Google Scholar
Liuba, K, Pronk, CJ, Stott, SR, et al. Polyclonal T-cell reconstitution of X-SCID recipients after in utero transplantation of lymphoid-primed multipotent progenitors. Blood 2009;113(19):4790–8.Google Scholar
Pearce, RD, Kiehm, D, Armstrong, DT, et al. Induction of hemopoietic chimerism in the caprine fetus by intraperitoneal injection of fetal liver cells. Experientia 1989;45:307–8.Google Scholar
Westlake, VJ, Jolly, RD, Jones, BR, et al. Hematopoietic cell transplantation in fetal lambs with ceroid-lipofuscinosis. Am J Med Genet 1995;57:365–8.Google Scholar
Forestier, F, Daffos, F, Catherine, N, et al. Developmental hematopoiesis in normal human fetal blood. Blood 1991;77:2360–3.Google Scholar
Clerici, M, DePalma, L, Roilides, E, et al. Analysis of T helper and antigen-presenting cell functions in cord blood and peripheral blood leukocytes from healthy children of different ages. J Clin Invest 1993;91:2829–36.Google Scholar
Serushago, B, Issekutz, AC, Lee, SH, et al. Deficient tumor necrosis factor secretion by cord blood mononuclear cells upon in vitro stimulation with listeria monocytogenes. J Interferon Cytokine Res 1996;16:381–7.Google Scholar
Weston, WL, Carson, BS, Barkin, RM, et al. Monocyte-macrophage function in the newborn. Am J Dis Child 1977;131:1241–2.Google Scholar
Uksila, J, Lassila, O, Hirvonen, T, et al. Development of natural killer cell function in the human fetus. J Immunol 1983;130:153–6.Google Scholar
Thilaganathan, B, Abbas, A, Nicolaides, KH. Fetal blood natural killer cells in human pregnancy. Fetal Diagn Ther 1993;8:149–53.Google Scholar
Renda, MC, Fecarotta, E, Dieli, F, et al. Evidence of alloreactive T lymphocytes in fetal liver: implications for fetal hematopoietic stem cell transplantation. Bone Marrow Transplant 2000;25:135–41.Google Scholar
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.Google Scholar
Toivanen, P, Uksila, J, Leino, A, et al. Development of mitogen responding T-cells and natural killer cells in the human fetus. Immunol Rev 1981;57:89–105.Google Scholar
Von Hoegen, P, Sarin, S, Krowka, JF. Deficiency in T-cell responses of human fetal lymph node cells: a lack of accessory cells. Immunol Cell Biol 1995;73:353–61.Google Scholar
Lindton, B, Markling, L, Ringden, O, et al. Mixed lymphocyte culture of human fetal liver cells. Fetal Diagn Ther 2000;15:71–8.Google Scholar
Thilaganathan, B, Nicolaides, KH, Mansur, CA, et al. Fetal b lymphocyte subpopulations in normal pregnancies. Fetal Diagn Ther 1993;8:15–21.Google Scholar
Anasetti, C, Amos, D, Beatty, PG, et al. Effect of hla compatibility on engraftment of bone marrow transplants in patients with leukemia or lymphoma. N Engl J Med 1989;320:197–204.Google Scholar
Beatty, PG, Clift, RA, Mickelson, EM, et al. Marrow transplantation from related donors other than HLA-identical siblings. N Engl J Med 1985;313:765–71.Google Scholar
Jankowski, RA, Ildstad, ST. Chimerism and tolerance: from freemartin cattle and neonatal mice to humans. Hum Immunol 1997;52:155–61.Google Scholar
Medvinsky, A, Dzierzak, E. Definitive hematopoiesis is autonomously initiated by the AGM region. Cell 1996;86:897–906.Google Scholar
Taylor, PA, McElmurry, RT, Lees, CJ, et al. Allogenic fetal liver cells have a distinct competitive engraftment advantage over adult bone marrow cells when infused into fetal as compared with adult severe combined immunodeficient recipients. Blood 2002;99:1870–2.Google Scholar
Chen, BJ, Cui, X, Sempowski, GD, et al. A comparison of murine T-cell-depleted adult bone marrow and full-term fetal blood cells in hematopoietic engraftment and immune reconstitution. Blood 2002;99(1):364–71.Google Scholar
Tocci, A, Roberts, IA, Kumar, S, et al. CD34+ cells from first-trimester fetal blood are enriched in primitive hemopoietic progenitors. Am J Obstet Gynecol 2003;188:1002–10.Google Scholar
Clapp, DW, Freie, B, Lee, WH, et al. Molecular evidence that in situ-transduced fetal liver hematopoietic stem/progenitor cells give rise to medullary hematopoiesis in adult rats. Blood 1995;86:2113–22.Google Scholar
Wagers, AJ, Christensen, JL, Weissman, IL. Cell fate determination from stem cells. Gene Ther 2002;9:606–12.Google Scholar
Rollini, P, Kaiser, S, Faes-van’t Hull, E, et al. Long-term expansion of transplantable human fetal liver hematopoietic stem cells. Blood 2004;103:1166–70.Google Scholar
Harrison, DE, Zhong, RK, Jordan, CT, et al. Relative to adult marrow, fetal liver repopulates nearly five times more effectively long-term than short-term. Exp Hematol 1997;25:293–7.Google Scholar
Taylor, PA, McElmurry, RT, Lees, CJ, et al. Allogenic fetal liver cells have a distinct competitive engraftment advantage over adult bone marrow cells when infused into fetal as compared with adult severe combined immunodeficient recipients. Blood 2002;99:1870–2.Google Scholar
Nicolini, FE, Holyoake, TL, Cashman, JD, et al. Unique differentiation programs of human fetal liver stem cells shown both in vitro and in vivo in NOD/SCID mice. Blood 1999;94:2686–95.Google Scholar
Rebel, VI, Miller, CL, Eaves, CJ, et al. The repopulation potential of fetal liver hematopoietic stem cells in mice exceeds that of their liver adult bone marrow counterparts. Blood 1996;87:3500–7.Google Scholar
Tocci, A, Roberts, IA, Kumar, S, et al. CD34+ cells from first-trimester fetal blood are enriched in primitive hemopoietic progenitors. Am J Obstet Gynecol 2003;188:1002–10.Google Scholar
Friedenstein, AJ, Petrakova, KV, Kurolesova, AI, et al. Heterotopic of bone marrow. Analysis of precursor cells for osteogenic and hematopoietic tissues. Transplantation 1968;6:230–47.Google Scholar
Pittenger, MF, Mackay, AM, Beck, SC, et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999;284:143–7.Google Scholar
Campagnoli, C, Roberts, IA, Kumar, S, et al. Identification of mesenchymal stem/progenitor cells in human first-trimester fetal blood, liver, and bone marrow. Blood 2001;98:2396–402.Google Scholar
Götherström, C, Ringdén, O, Westgren, M, et al. Immunomodulatory effects of human foetal liver-derived mesenchymal stem cells. Bone Marrow Transplant 2003;32:265–72.Google Scholar
In ‘t Anker, PS, Noort, WA, Kruisselbrink, AB, et al. Nonexpanded primary lung and bone marrow-derived mesenchymal cells promote the engraftment of umbilical cord blood-derived CD34(+) cells in NOD/SCID mice. Exp Hematol 2003;31:881–9.Google Scholar
Guillot, PV, Gotherstrom, C, Chan, J, et al. Human first-trimester fetal MSC express pluripotency markers and grow faster and have longer telomeres than adult MSC. Stem Cells 2007;25:646–54.Google Scholar
Götherström, C, West, A, Liden, J, et al. Difference in gene expression between human fetal liver and adult bone marrow mesenchymal stem cells. Haematologica 2005;90:1017–26.Google Scholar
Zhang, ZY, Teoh, SH, Chong, MS, et al. Superior osteogenic capacity for bone tissue engineering of fetal compared with perinatal and adult mesenchymal stem cells. Stem Cells 2009;27:126–37.Google Scholar
Guillot, PV, De Bari, C, Dell’Accio, F, et al. Comparative osteogenic transcription profiling of various fetal and adult mesenchymal stem cell sources. Differentiation 2008;76:946–57.Google Scholar
Chan, J, O’Donoghue, K, Gavina, M, et al. Galectin-1 induces skeletal muscle differentiation in human fetal mesenchymal stem cells and increases muscle regeneration. Stem Cells 2006;24:1879–91.Google Scholar
Chan, J, Waddington, SN, O’Donoghue, K, et al. Widespread distribution and muscle differentiation of human fetal mesenchymal stem cells after intrauterine transplantation in dystrophic mdx mouse. Stem Cells 2007;25:875–84.Google Scholar
Kennea, NL, Waddington, SN, Chan, J, et al. Differentiation of human fetal mesenchymal stem cells into cells with an oligodendrocyte phenotype. Cell Cycle 2009;8:1069–79.Google Scholar
In ‘t Anker, PS, Noort, WA, Scherjon, SA, et al. Mesenchymal stem cells in human second-trimester bone marrow, liver, lung, and spleen exhibit a similar immunophenotype but a heterogeneous multilineage differentiation potential. Haematologica 2003;88:845–52.Google Scholar
In ‘t Anker, PS, Scherjon, SA, Kleijburg-van der Keur, C, et al. Isolation of mesenchymal stem cells of fetal or maternal origin from human placenta. Stem Cells 2004;22:1338–45.Google Scholar
Hu, Y, Liao, L, Wang, Q, et al. Isolation and identification of mesenchymal stem cells from human fetal pancreas. J Lab Clin Med 2003;141:342–9.Google Scholar
Almeida-Porada, G, El Shabrawy, D, Porada, C, et al. Differentiative potential of human metanephric mesenchymal cells. Exp Hematol 2002;30:1454–62.Google Scholar
Götherström, C, Ringdén, O, Tammik, C, et al. Immunologic properties of human fetal mesenchymal stem cells. Am J Obstet Gynecol 2004;190:239–45.Google Scholar
Götherström, C, Lundqvist, A, Duprez, IR, et al. Fetal and adult multipotent mesenchymal stromal cells are killed by different pathways. Cytotherapy 2011;13:269–78.Google Scholar
Devine, SM, Cobbs, C, Jennings, M, et al. Mesenchymal stem cells distribute to a wide range of tissues following systemic infusion into nonhuman primates. Blood 2003;101:2999–3001.Google Scholar
Pereira, RF, Halford, KW, O’Hara, MD, et al. Cultured adherent cells from marrow can serve as long-lasting precursor cells for bone, cartilage, and lung in irradiated mice. Proc Natl Acad Sci U S A 1995;92:4857–61.Google Scholar
Le Blanc, K, Götherström, C, Ringdén, O, 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.Google Scholar
Carpenter, MK, Cui, X, Hu, ZY, et al. In vitro expansion of a multipotent population of human neural progenitor cells. Exp Neurol 1999;158:265–78.Google Scholar
Uchida, N, Buck, DW, He, D, et al. Direct isolation of human central nervous system stem cells. Proc Natl Acad Sci U S A 2000;97:14720–5.Google Scholar
Lindvall, O. Stem cells for cell therapy in Parkinson’s disease. Pharmacol Res 2003;47:279–87.Google Scholar
Lindvall, O, Björklund, A. Cell therapy in Parkinson’s disease. NeuroRx 2004;1:382–93.Google Scholar
Iwanami, A, Kaneko, S, Nakamura, M, et al. Transplantation of human neural stem cells for spinal cord injury in primates. J Neurosci Res 2005;80:182–90.Google Scholar
Cummings, BJ, Uchida, N, Tamaki, SJ, et al. Human neural stem cells differentiate and promote locomotor recovery in spinal cord-injured mice. Proc Natl Acad Sci U S A 2005;102:14069–74.Google Scholar
Akesson, E, Wolmer-Solberg, N, Cederarv, M, et al. Human neural stem cells and astrocytes, but not neurons, suppress an allogeneic lymphocyte response. Stem Cell Res 2009;2:56–67.Google Scholar
Choi, K, Kennedy, M, Kazarov, A, et al. A common precursor for hematopoietic and endothelial cells. Development 1998;125:725–32.Google Scholar
Nishikawa, SI, Nishikawa, S, Hirashima, M, et al. Progressive lineage analysis by cell sorting and culture identifies FLK1+VE-cadherin+ cells at a diverging point of endothelial and hemopoietic lineages. Development 1998;125:1747–57.Google Scholar
Javed, MJ, Mead, LE, Prater, D, et al. Endothelial colony forming cells and mesenchymal stem cells are enriched at different gestational ages in human umbilical cord blood. Pediatr Res 2008;64:68–73.Google Scholar
Ingram, DA, Mead, LE, Tanaka, H, et al. Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood. Blood 2004;104:2752–60.Google Scholar
Ruifrok, WP, de Boer, RA, Iwakura, A, et al. Estradiol-induced, endothelial progenitor cell-mediated neovascularization in male mice with hind-limb ischemia. Vasc Med 2009;14:29–36.Google Scholar
Oh, IY, Yoon, CH, Hur, J, et al. Involvement of E-selectin in recruitment of endothelial progenitor cells and angiogenesis in ischemic muscle. Blood 2007;110:3891–9.Google Scholar
Zheng, YW, Taniguchi, H. Diversity of hepatic stem cells in the fetal and adult liver. Semin Liver Dis 2003;23:337–48.Google Scholar
Strain, AJ, Crosby, HA, Nijjar, S, et al. Human liver-derived stem cells. Semin Liver Dis 2003;23:373–84.Google Scholar
Zalzman, M, Gupta, S, Giri, RK, et al. Reversal of hyperglycemia in mice by using human expandable insulin-producing cells differentiated from fetal liver progenitor cells. Proc Natl Acad Sci U S A 2003;100:7253–8.Google Scholar
Ilancheran, S, Moodley, Y, Manuelpillai, U. Human fetal membranes: a source of stem cells for tissue regeneration and repair? Placenta 2009;30:2–10.Google Scholar
Meller, D, Pires, RT, Mack, RJ, et al. Amniotic membrane transplantation for acute chemical or thermal burns. Ophthalmology 2000;107:980–9; discussion 990.Google Scholar
Tseng, SC, Prabhasawat, P, Barton, K, et al. Amniotic membrane transplantation with or without limbal allografts for corneal surface reconstruction in patients with limbal stem cell deficiency. Arch Ophthalmol 1998;116:431–41.Google Scholar
Pires, RT, Chokshi, A, Tseng, SC. Amniotic membrane transplantation or conjunctival limbal autograft for limbal stem cell deficiency induced by 5-fluorouracil in glaucoma surgeries. Cornea 2000;19:284–7.Google Scholar
Tiblad, E, Westgren, M. Fetal stem-cell transplantation. Best Pract Res Clin Obstet Gynaecol 2008;22:189–201.Google Scholar
Touraine, JL, Raudrant, D, Golfier, F, et al. Reappraisal of in utero stem cell transplantation based on long-term results. Fetal Diagn Ther 2004;19:305–12.Google Scholar
Bambach, BJ, Moser, HW, Blakemore, K, et al. Engraftment following in utero bone marrow transplantation for globoid cell leukodystrophy. Bone Marrow Transplant 1997;19:399–402.Google Scholar
Muench, MO, Rae, J, Barcena, A, et al. Transplantation of a fetus with paternal thy-1(+) cd34(+)cells for chronic granulomatous disease. Bone Marrow Transplant 2001;27:355–64.Google Scholar
Porta, F, Mazzolari, E, Zucca, S, et al. Prenatal transplant in a fetus affected by omenn syndrome. Bone Marrow Transplant 2000;25(S):S43.Google Scholar
Wengler, GS, Lanfranchi, A, Frusca, T, 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.Google Scholar
Hayward, A, Ambruso, D, Battaglia, F, et al. Microchimerism and tolerance following in utero transplantation and transfusion for alpha-thalassemia-1. Fetal Diagn Ther 1998;13:8–14.Google Scholar
Diukman, R, Golbus, MS. In utero stem cell therapy. J Reprod Med 1992;37:515–20.Google Scholar
Monni, G, Ibba, RM, Zoppi, MA, et al. In utero stem cell transplantation. Croat Med J 1998;39:220–3.Google Scholar
Slavin, S, Naparstek, E, Ziegler, M, et al. Clinical application of in utero bone marrow transplantation for treatment of genetic diseases-feasibility studies. Bone Marrow Transplant 1992;9 Suppl 1:189–90.Google Scholar
Touraine, JL, Raudrant, D, Golfier, F, et al. Reappraisal of in utero stem cell transplantation based on long-term results. Fetal Diagn Ther 2004;19:305–12.Google Scholar
Touraine, JL, Raudrant, D, Royo, C, et al. In utero transplantation of hemopoietic stem cells in humans. Transplant Proc 1991;23:1706–8.Google Scholar
Renda, MC, Daimiani, G, Fecarotta, E, et al. 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.Google Scholar
Flake, AW, Zanjani, ED. In utero hematopoietic stem cell transplantation. A status report. JAMA 1997;278:932–7.Google Scholar
Leung, W, Blakemore, K, Jones, RJ, et al. A human-murine chimera model for in utero human hematopoietic stem cell transplantation. Biol Blood Marrow Transplant 1999;5:1–7.Google Scholar

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