Perinatal stem-cell and gene therapy for hemoglobinopathies

Seminars in Fetal and Neonatal Medicine

Volumn 13, Issue 4, 2008, Pages 282-290

  Surbek, Daniel ^a   Schoeberlein, Andreina ^a   Wagner, Anna ^a  

^a UNIVERSITY OF BERN   (Switzerland)

Author keywords

Fetal gene therapy; Hemoglobinopathies; In utero transplantation; Stem cells

Indexed keywords

LENTIVIRUS VECTOR;

ARTICLE; ETHICS; EX VIVO GENE TRANSFER; GENE THERAPY; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEMOGLOBINOPATHY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; IMMUNE DEFICIENCY; IN UTERO STEM CELL TRANSPLANTATION; NONHUMAN; PATIENT SAFETY; PERINATAL CARE; PRENATAL DIAGNOSIS; RHESUS INCOMPATIBILITY; SOMATIC GENE THERAPY; STORAGE DISEASE;

ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; GENE THERAPY; HEMOGLOBINOPATHIES; HUMANS; PREGNANCY; STEM CELL TRANSPLANTATION;

EID: 44949149016     PISSN: 1744165X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.siny.2008.03.002     Document Type: Article

References (99)

1. Surbek D.V., and Holzgreve W. Why do we need noninvasive prenatal diagnosis?. In: Hahn S., and Holzgreve W. (Eds). Fetal cells and fetal DNA in maternal blood. New developments for a new millennium (2001), Karger, Basel, New York 21-27
2. Holzgreve W. Will ultrasound-screening and ultrasound-guided procedures be replaced by non-invasive techniques for the diagnosis of fetal chromosomal anomalies?. Ultrasound Obstet Gynecol 9 (1997) 217-219
3. Cheung M.C., Goldberg J.D., and Kan Y.W. Prenatal diagnosis of sickle cell anaemia and thalassaemia ba analysis of fetal cells in maternal blood. Nat Genet 14 (1996) 264-268
4. Li Y., Di Naro E., Vitucci A., et al. Detection of paternally inherited fetal point mutations for betal-thalassemai using size-fractionated cell-free DNA in maternal plasma. JAMA 293 (2005) 843-849
5. Buckley R.H., Schiff S.E., Schiff R.I., et al. Hematopoietic stem cell transplantation for the treatment of severe combined immunodeficiency syndrome. N Engl J Med 340 (1999) 508-516
6. Lucarelli G., Clift R.A., Galimberti M., et al. Bone marrow transplantation in adult thalassemic patients. Blood 93 (1999) 1164-1167
7. Shapiro E., Krivit W., Lockman L., et al. Long-term effect of bone-marrow transplantation for childhood-onset cerebral X-linked adreno-leukoldystrophy. Lancet 356 (2000) 713-718
8. Escolar M.L., Poe M.D., Provenzale J.M., et al. Transplantation of umbilical-cord blood in babies with infantile Krabbe's disease. N Engl J Med 352 (2005) 2069-2081
9. Tavian M., Coulombel L., Luton D., San Clemente H., Dieterlen-Lièvre F., and Péault B. Aorta-associated CD34+ hematopoietic cells in the early human embryo. Blood 87 (1996) 67-72
10. Blau C.A., and Stamatoyannopoulos G. Preemptive therapy for genetic disease. Nat Med 2 (1996) 161-162
11. Flake A.W., and Zanjani E.D. In utero hematopoietic stem cell transplantation: ontogenetic opportunities and biologic barriers. Blood 94 (1999) 2179-2191
12. Flake A.W., Roncarolo M.G., Puck J.M., Almeida-Porada G., Evans M.I., Johnson M.P., et al. Treatment of X-linked severe combined immunodeficiency by in utero transplantation of paternal bone marrow. N Engl J Med 335 (1996) 1806-1810
13. Pirovano S., Notarangelo L.D., Malacarne F., et al. Reconstitution of T-cell compartment after in utero stem cell transplantation: analysis of T-cell repertoire and thymic output. Haematologica 89 (2004) 450-461
14. 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 61 (1996) 1176-1179
15. Sanna M.A., Monni G., Ibba R.M., et al. In utero stem cell transplantation for beta-thalassemia:a case-report. Bone Marrow Transplant 23 (1999) S109
16. Bambach B.J., Moser H.W., Blakemore K., et al. Engraftment following in utero bone marrow transplantation for globoid cell leukodystrophy. Bone Marrow Transplant 19 (1997) 399-402
17. Surbek D.V., Gratwohl A., and Holzgreve W. In utero hematopoietic stem cell transfer: current status and future strategies. Eur J Obstet Gynecol Reprod Biol 85 (1999) 109-115
18. Milner R., Shaaban A., Kim H.B., Fichter C., and Flake A.W. Natural killer cells do not mediate allograft rejection after in utero hematopoietic stem cell transplantation. Blood 92 (1998) 288b
19. Peranteau W.H., Endo M., Adibe O.O., and Flake A.W. Evidence for an immune barrier after in utero hematopoietic-cell transplantation. Blood 109 (2007) 1331-1333
20. Troeger C., Surbek D., Schoeberlein A., et al. In utero hematopoietic stem cell transplantation - experiences in mice, sheep and humans. Swiss Med Wkly 136 (2007) 498-503
21. Zanjani E.D., Flake A.W., Rice H., Hedrick M., and Tavassoli M. Long-term repopulating ability of xenogeneic transplanted human liver hematopoietic stem cells in sheep. J Clin Invest 93 (1994) 1051
22. Young A., Holzgreve W., Dudler L., et al. Engraftment of human cord blood-derived stem cells in preimmune ovine fetuses after ultrasound-guided in utero transplantation. Am J Obstet Gynecol 189 (2003) 698-701
23. Shields L.E., Bryant E.M., Easterling T.R., and Andrews R.G. Fetal liver cell transplantation for the creation of lymphohematopoietic chimerism in fetal baboons. Am J Obstet Gynecol 173 (1995) 1157-1160
24. Archer D.R., Turner C.W., Yeager A.M., and Fleming W.H. Sustained multilineage engraftment of allogeneic hematopoietic stem cells in NOD/SCID mice after in utero transplantation. Blood 90 (1997) 3222-3229
25. Turner C.W., Archer D.R., Wong J., Yeager A.M., and Fleming W.H. In utero transplantation of human fetal haemopoietic cells in NOD/SCID mice. Br J Haematol 103 (1998) 326-334
26. Santolaya-Forgas J., Galan I., Deleon-Luis J., and Wolf R. A study to determine if human umbilical cord hematopoietic stem cells can survive in baboon extra-embryonic celomic fluid: a prerequisite for determining the feasibility of in-utero stem cell xeno-transplantation via celocentesis. Fetal Diagn Ther 22 2 (2007) 131-135
27. Almeida-Porada G., Porada C.D., Tran N., and Zanjani E.D. 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 95 (2000) 3620-3627
28. Schoeberlein A., Holzgreve W., Dudler L., Hahn S., and Surbek D.V. Tissue-specific engraftment after in utero transplantation of mesenchymal stem cells into sheep fetuses. Am J Obstet Gynecol (2005) 192
29. Portmann-Lanz B., Schoeberlein A., Huber A., et al. Placental mesenchymal stem cells as potential autologous graft for pre- and perinatal neuroregeneration. Am J Obstet Gynecol 194 (2006) 664-673
30. Portmann-Lanz B., and Surbek D. Placental mesenchymal stem cells. Am J Obstet Gynecol 196 (2007) e18-e19
31. Carrier E., Hae T., Busch M.P., and Cowan M.J. Induction of tolerance in nondefective mice after in utero transplantation of major histocompatibility complex-mismatched fetal hematopoietic stem cells. Blood 86 (1995) 4681-4690
32. Hayashi S., Peranteau W.H., Shaaban A.F., and Flake A.W. Complete allogeneic hematopoietic chimerism achieved by a combined strategy of in utero hematopoietic stem cell transplantation and postnatal donor lymphocyte infusion. Blood 100 3 (2002) 804-812
33. Peranteau W.H., Hayashi S., Hsieh M., Shaaban A.F., and Flake A.W. High-level allogeneic chimerism achieved by prenatal tolerance induction and postnatal nonmyeloablative bone marrow transplantation. Blood 100 (2002) 2225-2234
34. Petersen S.M., Gendelman M., Murphy K.M., et al. Use of T-cell antibodies for donor dosaging in a canine model of in utero hematopoietic stem cell transplantation. Fetal Diagn Ther 22 3 (2007) 175-179
35. Peranteau W.H., Endo M., Adibe O.O., Merchant A., Zoltick P.W., and Flake A.W. CD26 inhibition enhances allogeneic donor-cell homing and engraftment after in utero hematopoietic-cell transplantation. Blood 108 (2006) 4268-4274
36. Shields L.E., Gaur L., Delio P., Potter J., Sieverkropp A., and Andrews R.G. Fetal immune suppression as adjunctive therapy for in utero hematopoietic stem cell transplantation in nonhuman primates. Stem Cells 22 (2004) 759-769
37. Shields L.E., Gaur L.K., Gough M., Potter J., Sieverkropp A., and Andrews R.G. In utero hematopoietic stem cell transplantation in nonhuman primates: the role of T cells. Stem Cells 21 (2003) 304-314
38. Bhattacharyya S., Chawla A., Smith K., et al. Multilineage engraftment with minimal graft-versus-host disease following in utero transplantation of S-59 psoralen/ultraviolet A light treated, sensitized T cells and adult T cell-depleted bone marrow in fetal mice. J Immunol 169 (2002) 6133-6140
39. Shaaban A.F., Kim H.B., Gaur L., Liechty K.W., and Flake A.W. Prenatal transplantation of cytokine-stimulated marrow improves early chimerism in a resistant strain combination but results in poor long-term engraftment. Exp Hematol 34 (2006) 1278-1287
40. Norbeck O., Tolfvenstam T., Shields L.E., Westgren M., and Broliden K. Parvovirus B19 capsid protein VP2 inhibits hematopoiesis in vitro and in vivo: implications for therapeutic use. Exp Hematol 32 11 (2004) 1082-1087
41. Liechty K.W., MacKenzie T.C., Shaaban A.F., et al. Human mesenchymal stem cells engraft and demonstrate site-specific differentiation after in utero transplantation. Nat Med 6 (2000) 1282-1286
42. Le Blanc K., Gotherstrom C., Ringden O., et al. Fetal mesenchymal stem-cell engraftment in bone after in utero transplantation in a patient with severe osteogenesis imperfecta. Transplantation 79 11 (2005) 1607-1614
43. Horwitz E.M., Prockop D.J., Gordon P.L., et al. Clinical responses to bone marrow transplantation in children with severe osteogenesis imperfecta. Blood 97 (2001) 1227-1231
44. Surbek D.V., Holzgreve W., and Nicolaides K.H. Hematopoietic stem cell transplantation and gene therapy in the fetus: ready for clinical use?. Hum Reprod Update 7 (2001) 85-91
45. Surbek D., Schoeberlein A., and Portmann B. Advances in fetal gene therapy. Perinatology 8 (2006) 249-262
46. Anderson W.F. Human gene therapy. Nature 392 Suppl (1998) 25-30
47. Zanjani E.D., and Anderson W.F. Prospects for in utero human gene therapy. Science 285 (1999) 2084-2088
48. Manno C.S., Chew A.J., Hutchison S., et al. AAV-mediated factor IX gene transfer to skeletal muscle in patients with severe hemophilia B. Blood 101 (2003) 2963-2972
49. Kohn D.B., Hershfield M.S., Carbonaro D., et al. T lymhpocytes with a normal ADA gene accumulate after transplantation of transduced autologous umbilical cord blood CD34+ cells in ADA-deficient SCID neonates. Nat Med 4 (1998) 775-780
50. Cavazzana-Calvo M., Hacein-Bey S., de Saint Basile G., et al. Gene therapy of human severe combined immunodeficiency (SCID)-X1 disease. Science 288 (2000) 669-672
51. Buckley R.H. Gene therapy for human SCID: dreams become reality. Nat Med 6 (2000) 623-624
52. Hacein-Bey S., von Kalle C., Schmidt M., et al. A serious adverse event after successful gene therapy for X-linked severe combined immunodeficiency. N Engl J Med 348 (2003) 255-256
53. Hacein-Bey S., Von Kalle C., Schmidt M., et al. LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science 302 (2003) 415-419
54. Bestor T.H. Gene silencing as a threat to the success of gene therapy. J Clin Invest 105 (2000) 409-411
55. Qin L., Ding Y., Pahud D.R., Chang E., Imperiale M.J., and Bromberg J.S. Promotor attenuation in gene therapy: interferon-γ and tumor necrosis factor-α inhibit transgene expression. Hum Gene Ther 6 (1997) 1039
56. Bunting K.D., Sangster M.Y., Ihle J.N., and Sorrentino B.P. Restoration of lymphocyte function in Janus kinase 3-deficient mice by retroviral-mediated gene transfer. Nat Med 4 (1998) 58-64
57. Bhatia M., Bonnet D., Murdoch B., Gan O.I., and Dick J.E. A newly discovered class of human hematopoietic cells with SCID-repopulating activity. Nat Med 4 (1998) 1038-1045
58. Ziegler B.L., Valtieri M., Porada G.A., et al. KDR receptor: a key marker defining hematopoietic stem cells. Science 285 (1999) 1553-1558
59. Snyder R.O., Miao C., Meuse L., et al. Correction of hemophilia B in canine and murine models using recombinant adeno-associated viral vectors. Nat Med 5 (1999) 64-70
60. Herzog R.W., Yang E.Y., Couto L.B., et al. Long-term correction of canine hemophilia B by gene transfer of blood coagulation factor IX mediated by adeno-associated viral vector. Nat Med 5 (1999) 56-63
61. Abonour R., Williams D.A., Einhorn L., et al. Efficient retrovirus-mediated transfer of the multidrug resistance 1 gene into autologous human long-term repopulating hematopoietic stem cells. Nat Med 6 (2000) 652-658
62. Harrington J.J., Van Bokkelen G., Mays R.W., Gustashaw K., and Willard H.F. Formation of de novo centromeres and construction of first-generation human artificial microchromosomes. Nat Genet 15 (1997) 345-355
63. Naldini L., Blomer U., Gallay P., et al. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272 (1996) 263-267
64. Kafri T., Blomer U., Peterson D.A., Gage F.H., and Verma I.M. Sustained expression of genes delivered directly into liver and muscle by lentiviral vectors. Nat Genet 17 (1997) 314-317
65. Miyoshi H., Smith K.A., Mosier D.E., Verma I.M., and Torbett B.E. Transduction of human CD34+ cells that mediate long-term engraftment of NOD/SCID mice by HIV vectors. Science 283 (1999) 682-686
66. May C., Rivella S., Callegari J., et al. Therapeutic haemoglobin synthesis in beta-thalassaemic mice expressing lentivirus-encoded human beta-globin. Nature 406 (2000) 82-86
67. Larsen J.E., Morrow S.L., Happel L., Sharp J.F., and Cohen J.C. Reversal of cystic fibrosis phenotype in mice by gene therapy in utero. Lancet 349 (1997) 619-620
68. Hayashi S.I., Morishita R., Aoki M., et al. In vivo gene transfer of gene and oligo deoxynucleotides into skin of fetal rats by incubation in amniotic fluid. Gene Ther 3 (1996) 878-885
69. Woo Y.J., Raju G.P., Swain J.L., Richmond M.E., Gardner T.J., and Balice-Gordon R.J. In utero cardiac gene transfer via intraplacental delivery of recombinant adenovirus. Circulation 96 (1997) 3561-3569
70. Mason C.A.E., Bigras J.-L., O'Blenes S.B., et al. Gene transfer in utero biologically engineers a patent ductud arteriosus im lambs by arresting fibronectin-dependent neointimal formation. Nat Med 5 (1999) 176-182
71. Seppen J., van der Rijt R., Looije N., van Til N.P., and Lamers W.H. Oude Elferink RPJ. Long-term correction of bilirubin UDPglucuronyltransferase deficiency in rats by in utero lentiviral gene transfer. Mol Ther 8 (2003) 593-599
72. Jimenez D.F., Lee C.I., O'Shea C.E., Kohn D.B., and Tarantal A.F. HIV-1-derived lentiviral vectors and fetal route of administration on transgene biodistribution and expression in rhesus monkeys. Gene Ther 12 (2005) 821-830
73. Peebles D., Gregory L.G., David A., et al. Widespread and efficient marker gene expression in the airway epithelia of fetal sheep after minimally invasive tracheal application of recombinant adenovirus in utero. Gene Ther 11 (2004) 70-78
74. Tsukamoto M., Ochiya T., Yoshida S., Sugimura T., and Terada M. Gene transfer and expression in progeny after intravenous DNA injection into pregnant mice. Nat Genet 9 (1995) 243-248
75. Rucker M., Fraites Jr. T.J., Porvasnik S.L., et al. Rescue of enzyme deficiency in embryonic diaphragm in a mouse model of metabolic myopathy: Pompe disease. Development 131 (2004) 3007-3019
76. Waddington S., Nivsarkar M.S., Mistry A.R., et al. Permanent phenotypic correction of haemophilia B in immunocompetent mice by prenatal gene therapy. Blood 104 (2004) 2714-2721
77. Senut M.-C., Suhr S., and Gage F.H. Gene transfer to the rodent placenta in situ. A new strategy for delivering gene products to the fetus. J Clin Invest 101 (1998) 1565-1571
78. Coutelle C., Themis M., Waddington S.M., et al. Gene therapy progress and prospects: fetal gene therapy - first proofs of concept - some adverse effects. Gene Ther 12 (2005) 1601-1607
79. Schoeberlein A., Schatt S., Troeger C., Surbek D., Holzgreve W., and Hahn S. Engraftment kinetics of human cord blood and murine fetal liver stem cells following in utero transplantation into immunodeficient mice. Stem Cells Dev 13 (2004) 677-684
80. Coutelle C., Douar A.-M., Colledge W.H., and Froster U. The challenge of fetal gene therapy. Nat Med 1 (1995) 864-866
81. Wyrsch A., Dalle Carbonare V., Jansen W., et al. Preterm umbilical cord blood is enriched in early hematopoietic progenitors with expansion properties equal to term cord blood progenitors. Exp Hematol 27 (1999) 1338-1345
82. Luther-Wyrsch A., Costello E., Thali M., et al. Stable transduction with lentiviral vectors and amplification of immature hematopoietic progenitors from cord blood of preterm human fetuses. Hum Gene Ther 12 (2001) 377-389
83. Geiger H., Sick S., Bonifer C., and Müller A.M. Globin gene expression is reprogrammed in chimeras generated by injecting adult hematopoietic stem cells into mouse blastocysts. Cell 93 (1998) 1055-1065
84. Winkler A., Kiem H.-P., Shields L., Sun Q.-H., and Andrews R.G. Gene transfer into fetal baboon hematopoietic progenitor cells. Hum Gene Ther 10 (1999) 667-677
85. Lutzko C., Omori F., Abrams-Ogg A.C., et al. Gene therapy for canine alpha-L-iduronidase deficiency: in utero adoptive transfer of genetically corrected hematopoietic progenitors results in engraftment but not amelioration of disease. Hum Gene Ther 10 (1999) 1521-1532
86. Surbek D.V., Tercanli S., and Holzgreve W. Transabdominal first trimester embryofetoscopy as potential approach to early in utero stem cell transplantation and gene therapy. Ultrasound Obstet Gynecol 15 (2000) 302-307
87. Milner R., Shaaban A.F., Kim H.B., et al. Long term high level expression of donor hemoglobin after in utero HSC transplantation in thalassemic knockout mice - selective advantage for donor red cells. Blood 92 (1998) 696a
88. Allay J.A., Persons D.A., Galipeau J., et al. In vivo selection of retrovirally transduced hematopoietic stem cells. Nat Med 4 (1998) 1136-1143
89. Surbek D.V., Young A., Danzer E., Schoeberlein A., and Holzgreve W. Ultrasound-guided stem cell sampling from the early ovine fetus for prenatal ex-vivo gene therapy. Am J Obstet Gynecol 187 (2002) 960-963
90. Schoeberlein A., Holzgreve W., Dudler L., Hahn S., and Surbek D.V. In utero transplantation of autologous and allogeneic fetal liver stem cells in ovine fetuses. Am J Obstet Gynecol 191 (2004) 1030-1036
91. Porada C.D., Tran N., Eglitis M., et al. In utero gene therapy: transfer and longterm expression of the bacterial neo-r gene in sheep after direct injection of retroviral vectors into the preimmune fetus. Hum Gene Ther 9 (1998) 1571-1585
92. Themis M., Schneider H., Kiserud T., et al. Successful expression of beta-galactosidase and factor IX transgenes in fetal and neonatal sheep after ultrasound-guided percutaneous adenovirus vector administration into the umbilical vein. Gene Ther 6 (1999) 1239-1248
93. Lipshutz G.S., Sarkar R., Flebbe-Rehwaldt L., Kazazian H., and Gaensler K.M.L. Short-term correction of factor VIII deficiency in a murine model of hemophilia A after delivery of adenovirus murine factor VIII in utero. Proc Natl Acad Sci USA 96 (1999) 13324-13329
94. Persons D.A., Allay E.R., Sabatino D.E., et al. Functional requirements for phenotypic correction of murine beta-thalassemia: implications for human gene therapy. Blood 97 (2001) 3275-3282
95. Han X.D., Lin C., Chang J., Sadelain M., and Kan Y.W. Fetal gene therapy of alpha-thalassemia in a mouse model. Proc Natl Acad Sci USA 104 (2007) 9007-9011
96. King D., Shakespeare T., Nicholson R., Clarke A., and McLean S. Risks inherent in fetal gene therapy. Nature 397 (1999) 383
97. Themis M., Waddington S.N., Schmidt M., et al. Oncogenesis following delivery of a non-primate lentiviral gene therapy vector to fetal mice. Mol Ther 12 (2005) 763-771
98. Fletcher J.C., and Richter G. Human fetal gene therapy: moral and ethical questions. Hum Gene Ther 7 (1996) 1605-1614
99. Caplan A.L., and Wilson J.M. The ethical challenges of in utero gene therapy. Nat Genet 24 (2000) 107