In utero stem cell transplantation

Seminars in Reproductive Medicine

Volumn 24, Issue 5, 2006, Pages 348-357

  Westgren, Magnus ^a,b  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Fetal therapy; Fetal transplantation; Hematopoietic stem cell; Mesenchymal stem cell; Stem cell

Indexed keywords

CHIMERA; CONGENITAL DISORDER; DISEASE MODEL; HEMATOLOGIC DISEASE; HEMATOPOIETIC STEM CELL; HISTOINCOMPATIBILITY; HUMAN; IMMUNOPATHOLOGY; IN UTERO STEM CELL TRANSPLANTATION; METABOLIC DISORDER; OUTCOME ASSESSMENT; REVIEW;

ANIMALS; CHIMERISM; EMBRYONIC STEM CELLS; FEMALE; FETAL DISEASES; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; MESENCHYMAL STEM CELL TRANSPLANTATION; PREGNANCY; STEM CELL TRANSPLANTATION;

EID: 33845299531     PISSN: 15268004     EISSN: None     Source Type: Journal    
DOI: 10.1055/s-2006-952156     Document Type: Review

References (103)

1. Davies J. A case of haemolytic disease with congenital rubella. BMJ 1967;2:819-822
2. Touraine JL, Royo C, Roncarolo MG, Murray K, de Boutciller O. Unmatched stem cell transplantations as a possible alter-native to bone marrow transplantation. Transplant Proc 1989; 21:3197-3198
3. Flake AW, Roncarolo JM, Puck G, et al. Treatment of X-linked severe combined immunodeficiency by in utero transplantation of paternal bone marrow. N Engl J Med 1996;335: 1806-1810
4. Lanfranchini A, Neva A, Tettoni K, Veradi R, Mazzollari E, Wengler G. In utero transplantation (IUT) of parental CD34+ cells in patient affected by primary immunodeficiencies. Bone Marrow Transplant 1998;21:S127-S128
5. Westgren M, Ringdén 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;187:475-482
6. Shields LE, Lindton B, Andrews RG, Westgren M. Fetal hematopoietic stem cell transplantation: a challenge for the twenty-first century. J Hematother Stem Cell Res 2002;11:617-631
7. Flake AW. Genetic therapies for the fetus. Clin Obstet Gynecol 2002;45:684-696
8. Flake AW. In utero stem cell transplantation. Clin Obstet Gynecol 2002;45:941-958
9. Jolly RD, Thompson KG, Murphy CE, Manktelow BW, Bruere AN, Winchester BG. Enzyme replacement therapy - an experiment of nature in chimeric mannosidosis calf. Pediatr Res 1976;10:219-224
10. Owen RD. Immunogenetic consequences of vascular anastomoses between bovine twins. Science 1945;102:400-401
11. Jones MZ, Cavanagh KT, Kranich R, et al. Possible beta-mannosidosis chimera. Altered expression of metabolic perturbations. J Inherit Metab Dis 1993;16:1012-1023
12. Picus J, Aldrich WR, Levin NL. A naturally occurring bone-marrow-chimeric primate. I. Integrity of its immune system. Transplantation 1985;39:297-303
13. Howell JM, Dorling PR, Shelton JN, Taylor EG, Palmer DG, Di Marco PN. Natural bone marrow transplantation in cattle with Pompés disease. Neuromuscul Disord 1991;1:449-454
14. Emery D, McCullagh P. Immunological reactivity between chimeric cattle twins. I. Homograft reaction. Transplantation 1980;29:4-9
15. van Dijk BA, Boomsma DI, de Man AJ. Blood group chimerism in human multiple births is not rare. Am J Med Genet 1996;61:264-268
16. Hansen HE, Niebuhr E, Lomas C. Chimeric twins. T.S. and M.R. reexamined. Hum Hered 1984;34:127-130
17. 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 USA 1979;76:5736-5740
18. 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;86:4353-4366
19. Archer DR, Turner CW, Yeager AM, Fleming WH. Sustained multilineage engraftment of allogeneic hematopoietic stem cells in NOD/SCID mice after in utero transplantation. Blood 1997;90:3222-3229
20. Carrier E, Lee TH, Busch MP, Cowan MJ. Induction of tolerance in nondefective mice after in utero transplantation of major histocompatibility complex-mismatched fetal hematopoietic stem cells. Blood 1995;86:4681-4690
21. Hajdu K, Tanigawara S, McLean LK, Cowan MJ, Golbus MS. In utero allogeneic hematopoietic stem cell transplantation to induce tolerance. Fetal Diagn Ther 1996;11:241-248
22. Howson JK, Matloub YH, Vallera DA, Blazar BR. In utero engraftment of fully H-2-incompatible versus congenic adult bone marrow transferred into nonanemic or anemic murine fetal recipients. Transplantation 1993;56:709-716
23. Flake A, Harrison MR, Adzick NS, Zanjani ND. Transplantation of fetal hematopoietic stem cells in utero: the creation of hematopoietic chimeras. Science 1986;223:776-778
24. Zanjani ED, Ruthven A, Ruthven J, Shaft D, Smith D, Flake AW. In utero hematopoietic stem cell transplantation results in donor specific tolerance and facilitates postnatal "boosting" of donor cell levels. Blood 1994;84:100a
25. Zanjani ED, Almeida-Porada G, Ascensao JL, MacKintosh FR, Flake AW. Transplantation of hematopoietic stem cells in utero. Stem Cells 1997;15:79-93
26. 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;25:885-892
27. Westlake V, Jolly R, Jones B, et al. Hematopoietic cell transplantation in fetal lambs with ceroid-lipofuscinosis. Am J Med Genet 1995;57:365-368
28. Pearce RD, Kiehm D, Armstrong DT, et al. Induction of hematopoietic chimerism in the caprine fetus by intraperitoneal injection of fetal liver cells. Experientia 1989;45:307-308
29. 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;190:960-970
30. Harrison M. In utero transplantation of fetal liver hematopoietic stem cells in monkeys. Lancet 1989;2:1425-1427
31. Roodman GD, Kuehl TJ, Vandeberg OL, Muirhead DY. In utero bone marrow transplantation of fetal baboons with mismatched adult baboon marrow. Blood Cells 1991;17:367-375
32. 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
33. Cowan MJ, Tarantal AF, Capper J, Harrison M, Garovoy M. Long-term engraftment following in utero T cell-depleted parental marrow transplantation into fetal rhesus monkeys. Bone Marrow Transplant 1996;17:1157-1165
34. Shields LE, Gaur LK, Gough M, Potter J, Sieverkropp A, Andrews RG. In utero hematopoietic stem cell transplantation in nonhuman primates: the role of T cells. Stem Cells 2003;21:304-314
35. Shields LE, Andrews RG. In utero stem cell transplantation in non-human primates: the role of T-cell number. Am J Obstet Gynecol 2001;184:S2
36. Shields LE, Gauer L, Delio P, Potter J, Sieverkropp A, Andrews RG. Fetal immune suppression as adjunctive therapy for in utero hematopoietic stem cell transplantation in nonhuman primates. Stem Cells 2004;22:759-769
37. Kim HB, Shaaban AF, Milner R, et al. In utero bone marrow transplantation induces tolerance by a combination of clonal deletion and anergy. J Pediatr Surg 1999;34:726-730
38. 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
39. 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;25:293-297
40. Shields LE, Andrews RG, Westgren M, Broliden K. In vitro hematopoiesis is inhibited in humans and non-human primates by recombinant parvo virus capsid. Am J Obstet Gynecol 2000;182:S18
41. Norbeck O, Tolvenstam T, Shields LE, Westgren M, Broliden K. Parvovirus B19 capsid protein VP2 inhibits hematopoiesis in vitro and in vivo: implications for therapeutic use. Exp Hematol 2004;32:1082-1087
42. Almeida-Porada G, Flake AW, Glimp HA, Zanjani ED. Cotransplantation of stroma results in enhancement of engraftment and early expression of donor hematopoietic stem cells in utero. Exp Hematol 1999;27:1569-1575
43. Almeida-Porada G, Porada CD, Tran N, Zanjani ED. 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;95:3620-3627
44. Flake A, Zanjani E. In utero hematopoietic stem cell transplantation: ontogenic opportunities and biological barriers. Blood 1999;94:2179-2191
45. 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;25:135-141.
46. Toivanen P, Uksila J, Leino A, Lassila O, Hirvonen T, Ruuskanen O. Development of mitogen responding T cells and natural killer cells in the human fetus. Immunol Rev 1981;57:89-105
47. Sites DP, Carr MC, Fudenberg HH. Ontogeny of cellular immunity in the human fetus: development of responses to phytohemaglutinin and to allogeneic cells. Cell Immunol 1974;11:257-271
48. Lindton B, Markling L, Ringden O, Westgren M. In vitro studies of the role of CD3+ and CD56+ cells in fetal liver cell alloreactivity. Transplantation 2003;76(1):204-209
49. Götherström C, Johnsson AM, Mattsson J, Papadogiannakis N, Westgren M. Identification of maternal hematopoietic cells in a 2nd trimester fetus. Fetal Diagn Ther 2005;20:355-358
50. Burk R. Clinical utility in maximizing CD 34+ cell count in stem cell grafts. Stem Cells 1999;17:373-376
51. Shields LE, Andrews RG. Gestational age changes in circulating CD34+ hematopoietic stem/progenitor cells in fetal cord blood. Am J Obstet Gynecol 1998;178:931-937
52. Shields LE, Gaur L, Delio P, et al. The use of CD 34(+) mobilized peripheral blood as a donor cell source does not improve chimerism after in utero hematopoietic stem cell transplantation in non-human primates. J Med Primatol 2005;34 (4):201-208
53. Hayward A, Ambruso D, Battaglia F, et al. Microchimerism and tolerance following intrauterine transplantation and transfusion for alpha-thalassemia-1. Fetal Diagn Ther 1998;13:8-14
54. Westgren M, Ringdén O, Eik Nes S, et al. Lack of evidence of permanent engraftment after in utero fetal stem cell transplantation in congenital hemoglobinopathies. Transplantation 1996;61:1176-1179
55. Diukman R, Golbus M. In utero stem cell therapy. J Reprod Med 1992;37:515-520
56. 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;9:189-190
57. Touraine JL, Raudrant D, Royo C, et al. In utero transplantation of hematopoietic stem cells in humans. Transplant Proc 1991;23:1706-1708
58. Peschle C. In utero transplantation of purified stem cells from an HLA-identical sibling into a beta-thalassemia embryo. Paper presented at: Second International Meeting for In Utero Stem Cell Transplantation and Gene Therapy, January 15, 1997; Nottingham, United Kingdom
59. Linch D, Rodeck C, Nicolaides K, Jones H, Brent L. Attempted bone-marrow transplantation in a 17-week fetus. Lancet 1986;2:1453
60. Thilaganathan B, Nicolaides KH, Morgan G. Subpopulations of CD34-positive hematopoietic progenitors in fetal blood. Br J Haematol 1994;87:634-636
61. Wengler GS, Lanfranchi T, Frusca R, et al. In-utero transplantation of parental CD34 hematopoietic progenitor cells in a patient with X-linked severe combined immunodeficiency (SCIDXI). Lancet 1996;348:1484-1487
62. Muench MO, Rae I, Barcena A, et al. Transplantation of a fetus with paternal Thy-1(+)CD34(+)cells for chronic granulomatous disease. Bone Marrow Transplant 2001;27:355-364
63. Porta F, Mazzolari E, Zucca S, et al. Prenatal transplant in a fetus affected by Omenn syndrome. Bone Marrow Transplant 2000;25(suppl):S43-44
64. Barnbusch BJ, Moser HW, Blakemore K, et al. Engraftment following in utero bone marrow transplantation for globoid cell leucodystrophy. BMT 1997;19:399-402
65. 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;5:1-7A
66. Flake AW, Zanjani ED. In utero hematopoietic stem cell transplantation. A status report. JAMA 1997;278:932-937
67. Friedenstein AJ, Petrakova KV, Kuroksova AI, et al. Heterotopic transplants of bone marrow: analysis of precursor cells for osteogenic and hematopoietic tissue. Transplantation 1968;6:230-247
68. Prockop DJ. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 1997;276:71-74
69. Haynesworth SE, Goshima J, Goldberg VM, et al. Characterization of cells with osteogenic potential from human marrow. Bone 1992;13:81-88
70. Devine SM, Cobbs C, Jennings M, Bartholomew A, Hoffman R. Mesenchymal stem cells distribute to a wide range of tissues following systemic infusion into non-human primates. Blood 2003;101:2999-3001
71. Pittenger MF, Mackay AM, Beck SC, et al. Multi-lineage potential of adult human mesenchymal stem cells. Science 1999;284:143-147
72. In't Anker PS, Scherjon SA, Kleijburg-van der Keur C, et al. Amniotic fluid as a novel source of mesenchymal stem cells for therapeutic transplantation. Blood 2003;102:1548-1549
73. Erices A, Conget P, Minguell JJ. Mesenchymal progenitor cells in human umbilical cord blood. Br J Haematol 2000;109:235-242
74. Lee OK, Kuo TK, Chen WM, Lee KD, Hsieh SL, Chen TH. Isolation of multi-potent mesenchymal stem cells from umbilical cord blood. Blood 2004;103:1669-1675
75. Pereira RF, Halford KW, O'Hara MD, et al. Cultured adherent cells from marrow can serve as long-lasting precursors for bone, cartilage, and lung in irradiated mice. Proc Natl Acad Sci USA 1995;92:4857-4861
76. Liechty KW, MacKenzie TC, Shaaban AF, et al. Human mesenchymal stem cells engraft and demonstrate site specific differentiation after in utero transplantation in sheep. Nat Med 2000;6:1282-1286
77. Migliaccio G, Migliaccio AR, Petti S, et al. Human embryonic hemopoiesis: kinetics of progenitors and precursors underlying the yolk sack-liver transition. J Clin Invest 1986;78:51-60
78. Zanjani ED, Ascensao JL, Tavasolli M. Liver-derived fetal hematopoietic stem cells selectively and preferentially home to fetal bone marrow. Blood 1993;81:399-404
79. Liechty KW, MacKenzie TC, Shaaban AF, et al. Human mesenchymal stem cells engraft and demonstrate site-specific differentiation after in utero transplantation in sheep. Nat Med 2000;6:1282-1286
80. 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;27:601-604
81. 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;192:1044-1052
82. Horwitz EM, Prockop DJ, Fitzpatrick LA, et al. Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta. Nat Med 1999;5:309-313
83. Horwitz EM, Gordon PL, Koo WK, et al. Isolated allogeneic bone marrow-derived mesenchymal cells engraft and stimulate growth in children with osteogenesism imperfecta. Proc Natl Acad Sci USA 2002;99:8932-8937
84. 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;79:1607-1614
85. Di Nicola M, Carlo-Stella C, Magni M, et al. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or non-specific mitogenic stimuli. Blood 2002;99:3838-3843
86. Götherström 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;190:239-245
87. Götherström C, Ringdén O, Westgren M, Tammik L, Le Blanc K. Immunomodulatory effects of human foetal liver-derived mesenchymal stem cells. Bone Marrow Transplant 2003;32:265-272
88. Götherström C, West A, Liden J, Uzunel M, Lahesmaa R, Le Blanc K. Difference in gene expression between human fetal liver and adult bone marrow mesenchymal stem cells. Haematologica 2005;90:1017-1026
89. Cubert R, Cheng EY, Mack S, et al. Osteogenesis imperfecta: mode of delivery and neonatal outcome. Obstet Gynecol 2001;97:66-69
90. Kaur C, Hao AJ, Wu CH, Ling EA. Origin of microglia. Microsc Res Tech 2001;54:2-9
91. Gussoni E, Blau HM, Kunkel LM. The fate of individual myoblasts after in utero transplantation into muscles of DMD patients. Nat Med 1997;3:970-977
92. De Bari C, Delláccio F, Vandenabeele F, et al. Skeletal muscle repair by adult human mesenchymal stem cells from synovial membrane. J Cell Biol 2003;160:909-918
93. In't Anker P, Noort W, Scherjon S, et al. Mesenchymal stem cells in human second trimester bone marrow, liver, lung, and spleen exhibit a similar immunophenotype but a heterogenous multilineage differentiation potential. Haematologica 2003;88:845-852
94. In't Anker P, Noort WA, Kruisserbrink AB, et al. Nonexpanded primary lung and bone marrow derived mesenchymal cells promote the engraftment of umbilical cord blood derived CD 34+ cells in NOD/SCID mice. Exp Hematol 2003;31:881-889
95. 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;98:2396-2402
96. Sasaki K, Nagao Y, Kitano Y, et al. Hematopoietic microchimerism in sheep after in utero transplantation of cultured cynomolgus embryonic stem cells. Transplantation 2005;79 (1):32-37
97. Nava S, Westgren M, Jakesh M, et al. Characterization of cells in the developing human liver. Differentiation 2005;73:249-260
98. Nowak G, Ericzon BG, Nava S, Jakesch M, Westgren M, Sumitral-Holgersson S. Identification of expandable human progenitors which differentiate into mature hepatic cells in vivo. Gut 2005;54:972-979
99. Orlandi F, Giambona A, Messana F, et al. Evidence of induced non-tolerance in HLA-identical twins with hemoglobinopathy after in utero fetal transplantation. Bone Marrow Transplant 1996;18:637-639
100. Thilaganthan B, Nicoliades K. Intrauterine bone-marrow transplantation a gestation. Lancet 1993;342:243
101. Touraine JL, Raudrant D, Laplace S. Transplantation of hematopoietic cells from the fetal liver to treat patients with congenital diseases postnatally or prenatally. Transplant Proc 1997;29:712-713
102. 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
103. Monni G, Ibba RM, Zoppi MA, Floris M. In utero stem cell transplantation. Croat Med J 1998;39:220-223