In utero hematopoietic stem cell transplantation: Ontogenic opportunities and biologic barriers

Blood

Volumn 94, Issue 7, 1999, Pages 2179-2191

  Flake, Alan W ^a   Zanjani, Esmail D ^b  

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

FETUS; FETUS RISK; GRAFT REJECTION; HEMATOLOGIC DISEASE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEMATOPOIETIC SYSTEM; HUMAN; MAJOR HISTOCOMPATIBILITY COMPLEX; NONHUMAN; ONTOGENY; PRENATAL DEVELOPMENT; PRIORITY JOURNAL; REVIEW; TREATMENT OUTCOME;

EID: 0033215518     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood.v94.7.2179.419k43_2179_2191     Document Type: Review

References (136)

1. Flake AW, Zanjani ED: In utero transplantation of hematopoietic stem cells. Crit Rev Oncol Hematol 15:35, 1993
2. Flake AW, Zanjani ED: In utero hematopoietic stem cell transplantation. A status report. JAMA 278:932, 1997
3. Owen RD: Immunogenetic consequences of vascular anastomoses between bovine cattle twins. Science 102:400, 1945
4. Simonsen M: The acquired immunity concept in kidney Homotransplantation. Ann NY Acad Sci 59:448, 1955
5. Cragle R, Stone W: Preliminary results of kidney grafts between cattle chimeric twins. Transplantation 5:328, 1967
6. Gill T: Chimerism in humans. Transplant Proc 9:1423, 1977
7. van Dijk B, Bommsma D, de Man A: Blood group chimerism in human multiple births is not rare. Am J Med Genet 61:264, 1996
8. Picus J, Aldrich WR, Letvin NL: A naturally occurring bone-marrow-chimeric primate. I. Integrity of its immune system. Transplantation 39:297, 1985
9. Picus J, Holley K, Aldrich WR, Griffin JD, Letvin NL: A naturally occurring bone marrow-chimeric primate. II. Environment dictates restriction on cytolytic T lymphocyte-target cell interactions. J Exp Med 162:2035, 1985
10. Flake AW, Harrison MR, Adzick NS, Zanjani ED: Transplantation of fetal hematopoietic stem cells in utero: The creation of hematopoietic chimeras. Science 233:776, 1986
11. Zanjani ED, Ascensao JL, Flake AW, Harrison MR, Tavassoli M: The fetus as an optimal donor and recipient of hemopoietic stem cells. Bone Marrow Transplant 10:107, 1992 (suppl 1)
12. Zanjani ED, Pallavicini MG, Flake AW, Ascensao JL, Langlois RG, Reitsma M, MacKintosh FR, Stutes D, Harrison MR, Tavassoli M: Engraftment and long-term expression of human fetal hemopoietic stem cells in sheep following transplantation in utero. J Clin Invest 89:1178, 1992
13. Srour EF, Zanjani ED, Brandt JE, Leemhuis T, Briddell RA, Heerema NA, Hoffman R: Sustained human hematopoiesis in sheep transplanted in utero during early gestation with fractionated adult human bone marrow cells. Blood 79:1404, 1992
14. Srour EF, Zanjani ED, Cornetta K, Traycoff CM, Flake AW, Hedrick M, Brandt JE, Leemhuis T, Hoffman R: Persistence of human multilineage, self-renewing lymphohematopoietic stem cells in chimeric sheep. Blood 82:3333, 1993
15. Civin CJ, Lee MJ, Hedrick M, Rice H, Zanjani ED: Purified CD34+/lineage-/38-cells contain hematopoeitic stem cells. Blood 82:180a, 1993 (abstr, suppl 1)
16. Kawashima I, Zanjani E, Almaida-Porada G, Flake A, Zeng H, Ogawa M: CD34+ human marrow cells that express low levels of Kit protein are enriched for long-term marrow-engrafting cells. Blood 87:4136, 1996
17. Yin AH, Miraglia S, Zanjani ED, Almeida-Porada G, Ogawa M, Leary AG. Olweus J, Kearney J, Buck DW: AC133, a novel marker for human hematopoietic stem and progenitor cells. Blood 90:5002, 1997
18. Zanjani ED, Almeida-Porada G, Livingston AG, Flake AW, Ogawa M: Human bone marrow CD34-cells engraft in vivo and undergo multilineage expression that includes giving rise to CD34+ cells. Exp Hematol 26:353, 1998
19. Zanjani ED, Flake AW, Rice H, Hedrick M, Tavassoli M: Long-term repopulating ability of xenogeneic transplanted human fetal liver hematopoietic stem cells in sheep. J Clin Invest 93:1051, 1994
20. Harrison MR, Slotnick RN, Crombleholme TM, Golbus MS, Tarantal AF, Zanjani ED: In-utero transplantation of fetal liver haemopoietic stem cells in monkeys. Lancet 2:1425, 1989
21. Pearce R, Kiehm D, Armstrong D, Little P, Callahan J, Klunder L, Clarke J: Induction of hematopoietic chimerism in the caprine fetus by intraperitoneal injection of fetal liver cells. Experientia 45:307, 1989
22. Rice HE, Hedrick MH, Flake AW: In utero transplantation of rat hematopoietic stem cells induces xenogeneic chimerism in mice. Transplant Proc 26:126, 1994
23. Pallavicini MG, Flake AW, Madden D, Bethel C, Duncan B, Gonzalgo ML, Haendel S, Montoya T, Roberts L: Hemopoietic chimerism in rodents transplanted in utero with fetal human hemopoietic cells. Transplant Proc 24:542, 1992
24. 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 86:4681, 1995
25. Carrier E, Lee TH, Busch MP, Cowan MJ: Recruitment of engrafted donor cells postnatally into the blood with cytokines after in utero transplantation in mice. Transplantation 64:627, 1997
26. Kim HB, Shaaban AF, Yang EY, Liechty KW, Flake AW: Microchimerism and tolerance after in utero bone marrow transplantation in mice. J Surg Res 77:1, 1998
27. Fleischman R, Mintz B: Prevention of genetic anemias in mice by microinjection of normal hematopoietic cells into the fetal placenta. Proc Natl Acad Sci USA 76:5736, 1979
28. Russell ES: Hereditary anemias of the mouse. A review for geneticists. Adv Genet 20:357, 1979
29. Blazar BR, Taylor PA, Vallera DA: Adult bone marrow-derived pluripotent hematopoietic stem cells are engraftable when transferred in utero into moderately anemic fetal recipients. Blood 85:833, 1995
30. 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 86:4353, 1995
31. Blazar BR, Taylor PA, McElmurry R, Tian L, Panoskaltsis-Mortari A, Lam S, Lees C, Waldschmidt T, Vallera DA: Engraftment of severe combined immune deficient mice receiving allogeneic bone marrow via in utero or postnatal transfer. Blood 92:3949, 1998
32. 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 90:3222, 1997
33. Shultz LD, Schweitzer PA, Christianson SW, Gott B, Schweitzer IB, Tennent B, McKenna S, Mobraaten L, Rajan TV, Greiner DL: Multiple defects in innate and adaptive immunologic function in NOD/LtSz-scid mice. J Immunol 154:180, 1995
34. Diukman R, Golbus MS: In utero stem cell therapy. J Reprod Med 37:515, 1992
35. Cowan M, Golbus M: In utero hematopoietic stem cell transplants for inherited disease. Am J Pediatr Hematol Oncol 16:35, 1994
36. Touraine JL, Raudrant D, Royo C, Rebaud A, Roncarolo MG, Souillet G, Philippe N, Touraine F, Betuel H: In-utero transplantation of stem cells in bare lymphocyte syndrome. Lancet 1:1382, 1989
37. Touraine JL, Raudrant D, Rebaud A, Roncarolo MG, Laplace S, Gebuhrer L, Betuel H, Frappaz D, Freycon F, Zabot MT, Dubernard JM: In utero transplantation of stem cells in humans: Immunological aspects and clinical follow-up of patients. Bone Marrow Transplant 1:121, 1992
38. Flake A, Roncarolo M-G, Puck J, Almeida-Porada G, Evans M, Johnson M, Abella E, Harrison D, Zanjani E: Treatment of X-linked severe combined immunodeficiency by in utero transplantation of paternal bone marrow. N Engl J Med 335:1806, 1996
39. Wengler G, Lanfranchi A, Frusca T, Verardi R, Neva A, Brugnoni D, Gilliani S, Fiorini M, Mella P, Guandalini F, Mazzolari E, Pecorelli S, Notarangelo L, Porta F, Ugazio A: In-utero transplantation of parental CD34 haematopoietic progenitor cells in a patient with X-linked severe combined immunodeficiency (SCIDX1). Lancet 348:1484, 1996
40. Touraine J: Treatment of human fetuses and induction of immunological tolerance in humans by in utero transplantation of stem cells into fetal recipients. Acta Haematol 96:115, 1996
41. Flake AW, Zanjani ED: Unpublished data, 1996
42. Harrison MR, Albanese C, Muench M, Farrell J, Lopoo J, Barcena A: Allogeneic in utero transplantation of CD34+THY-1+ bone marrow derived hematopoietic stem cells (HSC) in a fetus with chronic granulomatous disease. Proceedings of the International Fetal Medicine and Surgery Society. Carlisle, UK, 1999
43. Slavin S, Naparstek E, Ziegler M, Lewin A: Clinical application of intrauterine bone marrow transplantation for treatment of genetic disease - Feasibility studies. Bone Marrow Transplant 1:189, 1992
44. Westgren M, Ringden O, Sturla E-N, Sverker E, Anvret M, Brubakk A-M, The-Hung B, Giambona A, Kiserud T, Kjaeldgaard A, Maggio A, Markling L, Seiger A, Orlanke F: Lack of evidence of permanent engraftment after in utero fetal stem cell transplantation in congenital hemoglobinopathies. Transplantation 61:1176, 1996
45. Hayward A, Ambruso D, Battaglia F, Donlon T, Eddelman K, Giller R, Hobbins J, Hsia YE, Quinones R, Shpall E, Trachtenberg E, Giardina P: Microchimerism and tolerance following intrauterine transplantation and transfusion for α-thalassemia-1. Fetal Diagn Ther 13:8, 1998
46. Flake AW, Zanjani ED: In Utero Transplantation, in Forman SJ, Bloom KG, Thomas ED (eds): Hematopoietic Cell Transplantation (ed 2). Malden, MA, Blackwell Science, 1999, p 444
47. Bambach BJ, Moser HW, Blakemore K, Corson VL, Griffin CA, Noga SJ, Perlman EJ, Zuckerman R, Wenger DA, Jones RJ: Engraftment following in utero bone marrow transplantation for globoid cell leukodystrophy. Bone Marrow Transplant 19:399, 1997
48. Hill SA, Smith KA, Williams KB, Denekamp J: The fractionated response of mouse stroma after X-rays and neutrons: influence of early vs late expression of damage. Radiother Oncol 16:129, 1989
49. Bierkens JG, Hendry JH, Testa NG: The radiation response and recovery of bone marrow stroma with particular reference to long-term bone marrow cultures. Eur J Haematol 43:95, 1989
50. Grande T, Bueren JA: Involvement of the bone marrow stroma in the residual hematopoietic damage induced by irradiation of adult and young mice. Exp Hematol 22:1283, 1994
51. Shirota T, Tavassoli M: Alterations of bone marrow sinus endothelium induced by ionizing irradiation: Implications in the homing of intravenously transplanted marrow cells. Blood Cells 18:197, 1992
52. Heckmann M, Douwes K, Peter R, Degitz K: Vascular activation of adhesion molecule mRNA and cell surface expression by ionizing radiation. Exp Cell Res 238:148, 1998
53. Hendrikx PJ, Martens CM, Hagenbeek A, Keij JF, Visser JW: Homing of fluorescently labeled murine hematopoietic stem cells. Exp Hematol 24:129, 1996
54. Metcalf D, Moore MAS: Embryonic aspects of haemopoiesis, in Neuberger A, Tatum EL (eds): Haemopoietic Cells, vol 24, Frontiers in Biology. Amsterdam, The Netherlands, North-Holland, 1971
55. Tavian M, Coulombel L, Luton D, San Clemente H, Dieterlen-Lievre F, Peault B: Aorta-associated CD34+ hematopoietic cells in the early human embryo. Blood 87:67, 1996
56. Brecher G, Ansell JD, Micklem HS, Tjio JH, Cronkite EP: Special proliferative sites are not needed for seeding and proliferation of transfused bone marrow cells in normal syngeneic mice. Proc Natl Acad Sci USA 79:5085, 1982
57. Stewart FM, Crittenden RB, Lowry PA, Pearson-White S, Quesenberry PJ: Long-term engraftment of normal and post-5-fluorouracil murine marrow into normal nonmyeloablated mice. Blood 81:2566, 1993
58. Rao SS, Peters SO, Crittenden RB, Stewart FM, Ramshaw HS, Quesenberry PJ: Stem cell transplantation in the normal nonmyeloablated host: Relationship between cell dose, schedule, and engraftment. Exp Hematol 25:114, 1997
59. Ramshaw HS, Crittenden RB, Dooner M, Peters SO, Rao SS, Quesenberry PJ: High levels of engraftment with a single infusion of bone marrow cells into normal unprepared mice. Biol Blood Marrow Transplant 1:74, 1995
60. Abkowitz JL, Persik MT, Shelton GH, Ott RL, Kiklevich JV, Catlin SN, Guttorp P: Behavior of hematopoietic stem cells in a large animal. Proc Natl Acad Sci USA 92:2031, 1995
61. Lemischka IR, Raulet DH, Mulligan RC: Developmental potential and dynamic behavior of hematopoietic stem cells. Cell 45:917, 1986
62. Bradford GB, Williams B, Rossi R, Bertoncello I: Quiescence, cycling, and turnover in the primitive hematopoietic stem cell compartment. Exp Hematol 25:445, 1997
63. Harrison DE, Astle CM, Lerner C: Number and continuous proliferative pattern of transplanted primitive immunohematopoietic stem cells. Proc Natl Acad Sci USA 85:822, 1988
64. Pietrzyk ME, Priestley GV, Wolf NS: Normal cycling patterns of hematopoietic stem cell subpopulations: An assay using long-term in vivo BrdU infusion. Blood. 66:1460, 1985
65. Van Zant G, Holland BP, Eldridge PW, Chen JJ: Genotype-restricted growth and aging patterns in hematopoietic stem cell populations of allophenic mice. J Exp Med 171:1547, 1990
66. Van Zant G, Scott-Micus K, Thompson BP, Fleischman RA, Perkins S: Stem cell quiescence/activation is reversible by serial transplantation and is independent of stromal cell genotype in mouse aggregation chimeras. Exp Hematol 20:470, 1992
67. Harrison DE, Lerner C, Hoppe PC, Carlson GA, Alling D: Large numbers of primitive stem cells are active simultaneously in aggregated embryo chimeric mice. Blood 69:773, 1987
68. Wolf NS, Bertoncello I, Jiang D, Priestley G: Developmental hematopoiesis from prenatal to young-adult life in the mouse model. Exp Hematol 23:142, 1995
69. Harrison DE, Astle CM: Short- and long-term multilineage repopulating hematopoietic stem cells in late fetal and newborn mice: Models for human umbilical cord blood. Blood 90:174, 1997
70. Flake A, Zanjani E: Cellular therapy. New trends and controversies in fetal diagnosis and therapy. Obstet Gynecol Clin North Am 24:159, 1997
71. Flake AW, Hedrick MH, Rice HE, Tavassoli M, Zanjani ED: 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 23:252, 1995
72. 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 USA 81:7835, 1984
73. Fleischman RA: Engraftment of W/c-kit mutant mice is determined by stem cell competition, not by increased marrow 'space.' Exp Hematol 24:209, 1996
74. Stewart FM, Zhong S, Wuu J, Hsieh C-c, Nilsson SK, Quesenberry PJ: Lymphohematopoietic engraftment in minimally myeloablated hosts. Blood 91:3681, 1998
75. Mintz B, Palm J: Gene control of hematopoiesis. I. Erythrocyte mosaicism and permanent immunological tolerance in allophenic mice. J Exp Med 129:1013, 1969
76. Van Zant G, Chen JJ, Scott-Micus K: Developmental potential of hematopoietic stem cells determined using retrovirally marked allophenic marrow. Blood 77:756, 1991
77. Ishida T, Inaba M, Hisha H, Sugiura K, Adachi Y, Nagata N, Ogawa R, Good RA, Ikehara S: Requirement of donor-derived stromal cells in the bone marrow for successful allogeneic bone marrow transplantation. Complete prevention of recurrence of autoimmune diseases in MRL/MP-Ipr/Ipr mice by transplantation of bone marrow plus bones (stromal cells) from the same donor. J Immunol 152:3119, 1994
78. Hisha H, Nishino T, Kawamura M, Adachi S, Ikehara S: Successful bone marrow transplantation by bone grafts in chimericresistant combination. Exp Hematol 23:347, 1995
79. Hashimoto F, Sugiura K, Inoue K, Ikehara S: Major histocompatibility complex restriction between hematopoietic stem cells and stromal cells in vivo. Blood 89:49, 1997
80. Kaufman CL, Colson YL, Wren SM, Watkins S, Simmons RL, lldstad ST: Phenotypic characterization of a novel bone marrow-derived cell that facilitates engraftment of allogeneic bone marrow stem cells. Blood 84:2436, 1994
81. Gaines BA, Colson YL, Kaufman CL, lldstad S: Facilitating cells enable engraftment of purified fetal liver stem cells in allogeneic recipients. Exp Hematol 24:902, 1996
82. Billingham R, Brent L, Medawar PB: Actively acquired tolerance of foreign cells. Nature 172:603, 1953
83. Sprent J: Central tolerance of T cells. Int Rev Immunol 13:95, 1995
84. Goodnow C: Balancing immunity and tolerance: deleting and tuning lymphocyte repertoires. Proc Natl Acad Sci USA 93:2264, 1996
85. Sha WC, Nelson CA, Newberry RD, Krantz DM, Russell JH, Loh DY: Positive and negative selection of an antigen receptor on T-cells in transgenic mice. Nature 336:73, 1988
86. Schwartz R: Acquisition of immunologic self tolerance. Cell 57:1073, 1989
87. Blackman M, Kappler J, Marrack P: The role of the T-cell receptor in positive and negative selection of developing T-cells. Science 248:1335, 1990
88. Guidos CJ, Danska JS, G. FC, Weissman IL: T cell receptor-mediated negative selection of autoreactive T lymphocyte precursors occurs after commitment to the CD4 or CD8 lineages. J Exp Med 172:835, 1990
89. Weissman IL: Developmental switches in the immune system. Cell 76:207, 1994
90. Anderson D, Billingham R, Lampkin G, Medawar P: The use of skin grafting to distinguish between monozygotic and dizygotic twins in cattle. Heredity 5:379, 1951
91. Simonsen M: Artificial production of immunologic tolerance. Nature 175:763, 1955
92. Egdahl RH, Good RA, Varco RL: Studies in homograft and heterograft survival. Surgery 42:228, 1957
93. Hedrick MH, Rice HE, MacGillivray TE, Bealer JF, Zanjani ED, Flake AW: Hematopoietic chimerism achieved by in utero hematopoietic stem cell injection does not induce donor-specific tolerance for renal allografts in sheep. Transplantation 58:110, 1994
94. Kim HB, Shaaban AF, Milner R, Fichter C. Flake AW: In utero bone marrow transplantation induces tolerance by a combination of clonal deletion and anergy. J Pediatr Surg 34:726, 1999
95. Bjorgvinsdottir H, Ding C, Pech N, Gifford M, Li L, Dinauer M: Retroviral-mediated gene transfer of gp91phox into bone marrow cells rescues defect in host defense against Aspergillus fumigatus in murine X-linked chronic granulomatous disease. Blood 89:41, 1997
96. Almeida-Porada G, Flake AW, Zanjani ED: Co-transplantation of stroma results in enhancement of engraftment and early expression of donor hematopoietic stem cell in utero. Exp Hematol 1999 (in press)
97. Or R, Kapelushnik J, Naparstek E, Nagler A, Filon D, Oppenheim A, Amar A, Aker M, Samuel S, Slavin S: Second transplantation using allogeneic peripheral blood stem cells in a beta-thalassaemia major patient featuring stable mixed chimaerism. Br J Haematol 94:285, 1996
98. Rhoads G, Jackson L, Schlesselman S, de la Cruz FF, Desnick RJ, Golbus MS, Ledbetter DH, Lubs HA, Mahoney MJ, Pergament E: The safety and efficacy of chorionic villus sampling for early prenatal diagnosis of cytogenetic abnormalities. N Engl J Med 320:609, 1989
99. Nelson JL, Furst DE, Maloney S, Gooley T, Evans PC, Smith A, Bean MA, Ober C, Bianchi DW: Microchimerism and HLA-compatible relationships of pregnancy in scleroderma. Lancet 351:559, 1998
100. Buckley RH, Schiff RI, Schiff SE, Markert ML, Williams LW, Harville TO, Roberts JL, Puck JM: Human severe combined immunodeficiency: Genetic, phenotypic, and functional diversity in one hundred eight infants. J Pediatr 130:378, 1997
101. Buckley RH, Schiff SE, Schiff RI, Markert L, Williams LW, Roberts JL, Myers LA, Ward FE: Hematopoietic stem-cell transplantation for the treatment of severe combined immunodeficiency. N Engl J Med 340:508, 1999
102. Prchal JT, Carroll AJ, Prchal JF, Crist WM, Skalka HW, Gealy WJ, Harley J, Malluh A: Wiskott-Aldrich syndrome: Cellular impairments and their implication for carrier detection. Blood 56:1048, 1980
103. Puck JM, Siminovitch KA, Poncz M, Greenberg CR, Rottem M, Conley ME: Atypical presentation of Wiskott-Aldrich syndrome: diagnosis in two unrelated males based on studies of maternal T cell X chromosome inactivation. Blood 75:2369, 1990
104. Wengler G, Gorlin JB, Williamson JM, Rosen FS, Bing DH: Nonrandom inactivation of the X chromosome in early lineage hematopoietic cells in carriers of Wiskott-Aldrich syndrome. Blood 85:2471, 1995
105. Puck J, Krauss C, Puck S, Buckley R, Conley M: Prenatal test for X-linked severe combined immunodeficiency by analysis of maternal X-chromosome inactivation and linkage analysis. N Engl J Med 322:1063, 1990
106. Kvittengen EA, Rootwelt H, Brandtzaeg P, Bergan A, Berger R: Hereditary tyrosinemia type I. Self induced correction of the fumarylacetoacetase defect. J Clin Invest 91:1816, 1993
107. Hirschhorn R, Yang DR, Puck JM, Huie ML, Jiang CK, Kurlandsky LE: Spontaneous in vivo reversion to normal of an inherited mutation in a patient with adenosine deaminase deficiency. Nat Genet 13:290, 1996
108. D'Andrea AD, Grompe M: Molecular biology of Fanconi anemia: Implications for diagnosis and therapy. Blood 90:1725, 1997
109. Ellis NA, Lennon DJ, Proylcheva M, Aldadeff B, Henderson EE, German J: Somatic intragenic recombination within the mutated locus BLM can correct the high sister-chromatid exchange phenotype of Bloom Syndrome cells. Am J Hum Genet 57:1019, 1995
110. Aruffo A, Farrington M, Hollenbaugh D, Li X, Milatovich A, Nonoyama S, Bajorath J, Grosmaire LS, Stenkamp R, Neubauer M: The CD40 ligand, gp39, is defective in activated T cells from patients with X-linked hyper-IgM syndrome. Cell 72:291, 1993
111. Hollenbaugh D, Wu LH, Ochs HD, Nonoyama S, Grosmaire LS, Ledbetter JA, Noelle RJ, Hill H, Aruffo A: The random inactivation of the X chromosome carrying the defective gene responsible for X-linked hyper IgM syndrome (X-HIM) in female carriers of HIGM1. J Clin Invest 94:616, 1994
112. Flake AW, Zanjani ED: In utero transplantation for thalassemia. Ann NY Acad Sci 850:300, 1998
113. Lucarelli G, Galimberti M, Polchi P, Angellucci E, Baronciani D, Durazzi S, Giardini C, Nicolini G, Politi P, Albertini F: Bone Marrow Transplantation in Thalassemia. Hematol Oncol Clin North Am 5:549, 1991
114. Walters MC, Sullivan KM, O'Reilly RJ, Boulad F, Brockstein J, Blume K, Amylon M, Johnson FL, Klemperer M, Graham-Pole J, Storb R, Hansen JA: Bone marrow transplantation for thalassemia. The USA experience. Am J Pediatr Hematol Oncol 16:11, 1994
115. Walters MC, Patience M, Leisenring W, Eckman JR, Scott JP, Mentzer WC, Davies SC, Ohene-Frempong K, Bernaudin F, Matthews DC, Storb R, Sullivan KM: Bone marrow transplantation for sickle cell disease. N Engl J Med 335:369, 1996
116. Vellodi A, Picton S, Downie CJ, Eltumi M, Stevens R, Evans DI: Bone marrow transplantation for thalassaemia: experience of two British centres. Bone Marrow Transplant 13:559, 1994
117. Cao A, Rosatelli MC: Screening and prenatal diagnosis of the haemoglobinopathies. Baillieres Clin Haematol 6:263, 1993
118. Bunn H, Forget B: Hemoglobin structure, in: Hemoglobin: Molecular. Genetic, and Clinical Aspects. Philadelphia, PA, Saunders, 1986. p 13
119. Lam Y, Ghosh A, Tang M, Lee C, Sin S: Second-trimester hydrops fetalis in pregnancies affected by homozygous alpha thalassemia-1. Prenat Diagn 17:267, 1997
120. Bethel C, Murugesh D, Harrison M, Mohandas N, Rubin E: Selective erythroid replacement in murine β-thalassemia using fetal hematopoietic stem cells. Proc Natl Acad Sci USA 90:10120, 1993
121. van den Bos C, Kieboom D, van der Sluijs J, Baert M, Ploemacher R, Wagemaker G: Selective advantage of normal erythrocyte production after bone marrow transplantation of α-thalassemic mice. Exp Hematol 22:441, 1994
122. Milner R, Shaaban AF, Kim HB, Fichter C, Scully M, Asakura T, Flake AW: Long term high level expression of donor hemoglobin after in utero HSC transplantation in β-globin knockout mice -Selective advantage for donor red cells. Blood 92:696a, 1998 (abstr, suppl 1)
123. Andreani M, Manna M, Lucarelli G, Tonucci P, Agostinelli F, Ripalti M, Rapa S, Talevi N, Galimberti M, Nesci S: Persistence of mixed chimerism in patients transplanted for the treatment of thalassemia. Blood 87:3494, 1996
124. Kapelushnik J, Or R, Filon D, Nagler A, Cividalli G, Aker M, Naparstek E, Slavin S, Oppenheim A: Analysis of beta-globin mutations shows stable mixed chimerism in patients with thalassemia after bone marrow transplantation. Blood 86:3241, 1995
125. Shapiro EG, Lockman LA, Balthazor M, Krivit W: Neuropsychological outcomes of several storage diseases with and without bone marrow transplantation. J Inher Metabol Dis 18:413, 1995
126. Kaye E: Therapeutic approaches to lysosomal storage diseases. Curr Opin Pediatr 7:650, 1995
127. Imaizumi M, Gushi K, Kurobane I, Inoue S, Suzuki J, Koizumi Y, Suzuki H, Sato A, Gotoh Y, Haginoya K: Long-term effects of bone marrow transplantation for inborn errors of metabolism: A study of four patients with lysosomal storage diseases. Acta Paediatr Jpn 36:30, 1994
128. Peters C, Shapiro EG, Anderson J, Henslee-Downey PJ, Klemperer MR, Cowan MJ, Saunders EF, deAlarcon PA, Twist C, Nachman JB, Hale GA, Harris RE, Rozans MK, Kurtzberg J, Grayson GH, Williams TE, Lenarsky C, Wagner JE, Krivit W: Hurler syndrome: II. Outcome of HLA-genotypically identical sibling and HLA-haploidentical related donor bone marrow transplantation in fifty-four children. The Storage Disease Collaborative Study Group. Blood 91:2601, 1998
129. Westlake VJ, Jolly RD, Jones BR, Mellor DJ, Machon R, Zanjani ED, Krivit W: Hematopoietic cell transplantation in fetal lambs with ceroid-lipofuscinosis. Am J Med Genet 57:365, 1995
130. Barron K: The microglial cell. A historical review. J Neurolog Sci 134:57, 1995 (suppl)
131. Taylor RM, Wolfe JH: Decreased lysosomal storage in the adult MPS VII mouse brain in the vicinity of grafts of retroviral vector-corrected fibroblasts secreting high levels of beta-glucuronidase. Nat Med 3:771, 1997
132. Fletcher JC: Fetal therapy, ethics and public policies. Fetal Diagn Ther 7:158, 1992
133. McCullough L, Chervenek F: Ethics in Obstetrics and Gynecology. New York, NY, Oxford University Press, 1994
134. Davis J: A case of haemolytic disease with congenital rubella. Demonstrated at the royal postgraduate medical school. Br Med J 2:819, 1967
135. Linch D, Rodeck C, Nicolaides K: Attempted bone marow transplantation in a 17 week fetus. Lancet 1:1382, 1986
136. Thalaganthan B, Nicolaides K: Intrauterine bone-marrow transplantation at 12 weeks gestation. Lancet 342:243, 1993