Perinatal gene transfer to the liver

Current Pharmaceutical Design

Volumn 17, Issue 24, 2011, Pages 2528-2541

  Mckay, Tristan R ^a   Rahim, Ahad A ^b   Buckley, Suzanne M K ^b   Ward, Natalie J ^b   Chan, Jerry K Y ^c   Howe, Steven J ^d   Waddington, Simon N ^b  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Fetal gene therapy; Glycogen storage disease; Hemophilia; In utero gene therapy; Liver; Lysosomal storage disease; Mucopolysaccharidosis; Neonatal gene therapy; Viral vector

Indexed keywords

4 PHENYLBUTYRIC ACID; ADENOVIRUS VECTOR; BENZOIC ACID; BLOOD CLOTTING FACTOR 10; BLOOD CLOTTING FACTOR 8; GLUCURONOSYLTRANSFERASE 1A1; LENTIVIRUS VECTOR; PARVOVIRUS VECTOR; RETROVIRUS VECTOR;

ACIDEMIA; BLOOD CLOTTING DISORDER; CRIGLER NAJJAR SYNDROME; DIET RESTRICTION; ENZYME REPLACEMENT; EXCHANGE BLOOD TRANSFUSION; FABRY DISEASE; FETAL THERAPY; GENE THERAPY; GENE TRANSFER; GLUCOSE INFUSION; GLYCOGEN STORAGE DISEASE; GLYCOGEN STORAGE DISEASE TYPE 1; GROWTH DISORDER; HEMODIALYSIS; HEMOPHILIA; HEMOPHILIA A; HEMOPHILIA B; HUMAN; HUNTER SYNDROME; HURLER SYNDROME; HYPERTENSION; IMMUNOPATHOLOGY; KIDNEY DISEASE; LIVER CELL CARCINOMA; LIVER DISEASE; LIVER TRANSPLANTATION; LYSOSOME STORAGE DISEASE; MAPLE SYRUP URINE DISEASE; MAROTEAUX LAMY SYNDROME; MORQUIO SYNDROME; MUCOPOLYSACCHARIDOSIS; MUCOPOLYSACCHARIDOSIS TYPE 7; NEWBORN PERIOD; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; ORNITHINE TRANSCARBAMYLASE DEFICIENCY; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN RESTRICTION; RETROVIRUS; REVIEW; SANFILIPPO SYNDROME; UREA CYCLE DISORDER; VIRUS DNA CELL DNA INTERACTION;

ADENOVIRIDAE; ANIMALS; DEPENDOVIRUS; FEMALE; FETAL DISEASES; FETAL THERAPIES; GENE THERAPY; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; HUMANS; INFANT, NEWBORN; LENTIVIRUS; LIVER; PREGNANCY;

EID: 80053509954     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/138161211797247541     Document Type: Review

References (173)

1. Mehta V, Abi Nader, K, Waddington, SN, David, AL. Organ targeted prenatal gene therapy - how far are we? Prenat Diagn 2011; In Press.
2. [Mattar CN, Choolani, M, Biswas, A, Waddington, SN, Chan, JKY. Fetal gene therapy: Recent advances and current challenges. Expert Opin Biol Ther 2011; In Press.
3. Buckley SMK, Rahim, AA, Chan, JKY, et al. Recent advances in fetal gene therapy. Ther Deliv 2011; 2: 461-469.
4. [Santore MT, Roybal, JL, Flake, AW. Prenatal stem cell transplantation and gene therapy. Clin Perinatol 2009; 36: 451-71, xi.
5. Roybal JL, Santore, MT, Flake, AW. Stem cell and genetic therapies for the fetus. Semin Fetal Neonatal Med 2009.
6. Abbink P, Lemckert, AA, Ewald, BA, et al. Comparative seroprevalence and immunogenicity of six rare serotype recombinant adenovirus vaccine vectors from subgroups B and D. J Virol 2007; 81: 4654-63.
7. Wickham TJ, Mathias, P, Cheresh, DA, Nemerow, GR. Integrins alpha v beta 3 and alpha v beta 5 promote adenovirus internalization but not virus attachment. Cell 1993; 73: 309-19.
8. Tomko RP, Xu, R, Philipson, L. HCAR and MCAR: the human and mouse cellular receptors for subgroup C adenoviruses and group B coxsackieviruses. Proc Natl Acad Sci USA 1997; 94: 3352-6.
9. Bergelson JM, Cunningham, JA, Droguett, G, et al. Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science 1997; 275: 1320-3.
10. Waddington SN, McVey, JH, Bhella, D, et al. Adenovirus serotype 5 hexon mediates liver gene transfer. Cell 2008; 132: 397-409.
11. Kalyuzhniy O, Di Paolo, N, Silvestry, M, et al. Adenovirus serotype 5 hexon is critical for virus infection of hepatocytes in vivo. Proc Natl Acad Sci USA 2008; 105: 5483-5488.
12. Vigant F, Descamps, D, Jullienne, B, et al. Substitution of Hexon Hypervariable Region 5 of Adenovirus Serotype 5 Abrogates Blood Factor Binding and Limits Gene Transfer to Liver. Mol Ther 2008; 16: 1474-1480.
13. Parker AL, Waddington, SN, Nicol, CG, et al. Multiple vitamin Kdependent coagulation zymogens promote adenovirus-mediated gene delivery to hepatocytes in vitro and in vivo Blood 2006; 108: 2554-61.
14. Waddington SN, Parker, AL, Havenga, M, et al. Targeting of adenovirus serotype 5 (Ad5) and 5/47 pseudotyped vectors in vivo: A fundamental involvement of coagulation factors and redundancy of CAR binding by Ad5. J. Virol. 2007; 81: 9568-9571.
15. Alba R, Bradshaw, AC, Coughlan, L, et al. Biodistribution and retargeting of FX-binding ablated Ad5 vectors. Blood 2010; 116: 2656-2664.
16. Cerullo V, Pesonen, S, Diaconu, I, et al. Oncolytic adenovirus coding for granulocyte macrophage colony-stimulating factor induces antitumoral immunity in cancer patients. Cancer Res 2010; 70: 4297-309.
17. Small EJ, Carducci, MA, Burke, JM, et al. A phase I trial of intravenous CG7870, a replication-selective, prostate-specific antigen-targeted oncolytic adenovirus, for the treatment of hormone-refractory, metastatic prostate cancer. Mol Ther 2006; 14: 107-17.
18. Alba R, Bosch, A, Chillon, M. Gutless adenovirus: last-generation adenovirus for gene therapy. Gene Ther 2005; 12 Suppl 1: S18-27.
19. Suerth JD, Maetzig, T, Galla, M, Baum, C, Schambach, A. Selfinactivating alpharetroviral vectors with a split-packaging design. J Virol 2010; 84: 6626-35.
20. Trobridge GD, Miller, DG, Jacobs, MA, et al. Foamy virus vector integration sites in normal human cells. Proc Natl Acad Sci USA 2006; 103: 1498-503.
21. Baum C, Schambach, A, Bohne, J, Galla, M. Retrovirus vectors: toward the plentivirus? Mol Ther 2006; 13: 1050-63.
22. Miyanohara A, Yee, JK, Bouic, K, LaPorte, P, Friedmann, T. Efficient in vivo transduction of the neonatal mouse liver with pseudotyped retroviral vectors. Gene Ther 1995; 2: 138-42.
23. Themis M, Waddington, SN, Schmitt, M, et al. Oncogenesis following delivery of a non-primate lentiviral gene therapy vector to fetal and neonatal mice Mol Ther 2005; 12: 763-771.
24. Kang Y, Xie, L, Tran, DT, et al. Persistent expression of factor VIII in vivo following nonprimate lentiviral gene transfer. Blood 2005.
25. Eglitis MA, Kantoff, P, Gilboa, E, Anderson, WF. Gene expression in mice after high efficiency retroviral-mediated gene transfer. Science 1985; 230: 1395-8.
26. Burns JC, Friedmann, T, Driever, W, Burrascano, M, Yee, JK. Vesicular stomatitis virus G glycoprotein pseudotyped retroviral vectors: concentration to very high titer and efficient gene transfer into mammalian and nonmammalian cells. Proc Natl Acad Sci USA 1993; 90: 8033-7.
27. Naldini L, Blomer, U, Gallay, P, et al. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 1996; 272: 263-7.
28. VandenDriessche T, Thorrez, L, Naldini, L, et al. Lentiviral vectors containing the human immunodeficiency virus type-1 central polypurine tract can efficiently transduce nondividing hepatocytes and antigen-presenting cells in vivo. Blood 2002; 100: 813-22.
29. Olsen JC. Gene transfer vectors derived from equine infectious anemia virus. Gene Ther 1998; 5: 1481-7.
30. Waddington SN, Mitrophanous, KA, Ellard, F, et al. Long-term transgene expression by administration of a lentivirus-based vector to the fetal circulation of immuno-competent mice. Gene Ther 2003; 10: 1234-40.
31. Grinshpun A, Condiotti, R, Waddington, S, et al. Neonatal gene therapy of glycogen storage disease type Ia using a feline immunodeficiency virus based vector. Mol Ther 2010; 18: 1592-1598.
32. Wu X, Li, Y, Crise, B, Burgess, SM. Transcription start regions in the human genome are favored targets for MLV integration. Science 2003; 300: 1749-51.
33. Banasik MB, McCray, PB, Jr. Integrase-defective lentiviral vectors: progress and applications. Gene Ther 2010; 17: 150-7.
34. Apolonia L, Waddington, SN, Fernandez, C, et al. Stable Gene Transfer to Muscle using Non-Integrating Lentiviral Vectors. Mol Ther 2007; 15: 1947-1954.
35. Matrai J, Cantore, A, Bartholomae, CC, et al. Hepatocyte-targeted expression by integrase-defective lentiviral vectors induces antigen-specific tolerance in mice with low genotoxic risk. Hepatology 2011; 53: 1696-707.
36. Grieger JC, Samulski, RJ. Adeno-associated virus as a gene therapy vector: vector development, production and clinical applications. Adv Biochem Eng Biotechnol 2005; 99: 119-45.
37. Gao G, Vandenberghe, LH, Alvira, MR, et al. Clades of Adenoassociated viruses are widely disseminated in human tissues. J Virol 2004; 78: 6381-8.
38. Gao G, Alvira, MR, Somanathan, S, et al. Adeno-associated viruses undergo substantial evolution in primates during natural infections. Proc Natl Acad Sci USA 2003; 100: 6081-6.
39. Nakai H, Storm, TA, Kay, MA. Recruitment of single-stranded recombinant adeno-associated virus vector genomes and intermolecular recombination are responsible for stable transduction of liver in vivo. J Virol 2000; 74: 9451-63.
40. McCarty DM, Fu, H, Monahan, PE, et al. Adeno-associated virus terminal repeat (TR) mutant generates self-complementary vectors to overcome the rate-limiting step to transduction in vivo. Gene Ther 2003; 10: 2112-8.
41. McCarty DM, Monahan, PE, Samulski, RJ. Self-complementary recombinant adeno-associated virus (scAAV) vectors promote efficient transduction independently of DNA synthesis. Gene Ther 2001; 8: 1248-54.
42. Martino AT, Suzuki, M, Markusic, DM, et al. The genome of selfcomplementary AAV vectors increases TLR9-dependent innate immune responses in the liver. Blood 2011.
43. Lipshutz GS, Gruber, CA, Cao, Y, et al. In utero delivery of adenoassociated viral vectors: intraperitoneal gene transfer produces long-term expression. Mol Ther 2001; 3: 284-92.
44. Paulk NK, Wursthorn, K, Wang, Z, et al. Adeno-associated virus gene repair corrects a mouse model of hereditary tyrosinemia in vivo. Hepatology 2010; 51: 1200-8.
45. Argyros O, Ping Wong, S, Niceta, M, et al. Persistent episomal transgene expression in liver following delivery of a scaffold/matrix attachment region containing non-viral vector. Gene Ther 2008; 15: 1593-1605.
46. Miao CH, Ye, X, Thompson, AR. High-level factor VIII gene expression in vivo achieved by nonviral liver-specific gene therapy vectors. Hum Gene Ther 2003; 14: 1297-305.
47. Wong SP, Argyros, O, Howe, SJ, Harbottle, RP. Systemic gene transfer of polyethylenimine (PEI)-plasmid DNA complexes to neonatal mice. J Control Release 2011; 150: 298-306.
48. Biron-Andreani C, Bezat-Bouchahda, C, Raulet, E, et al. Secretion of functional plasma haemostasis proteins in long-term primary cultures of human hepatocytes. Br J Haematol 2004; 125: 638-46.
49. [Tatsumi K, Ohashi, K, Taminishi, S, et al. Regulation of coagulation factors during liver regeneration in mice: Mechanism of factor VIII elevation in plasma. Thromb Res 2011; In Press.
50. Hoffman MM, Monroe, DM. Rethinking the coagulation cascade. Curr Hematol Rep 2005; 4: 391-6.
51. Petrus I, Chuah, M, Vandendriessche, T. Gene therapy strategies for hemophilia: benefits versus risks. J Gene Med 2010; 12: 797-809.
52. High KA. Update on progress and hurdles in novel genetic therapies for hemophilia. Hematology Am Soc Hematol Educ Program 2007; 2007: 466-72.
53. Manno CS, Arruda, VR, Pierce, GF, et al. Successful transduction of liver in hemophilia by AAV-Factor IX and limitations imposed by the host immune response. Nat Med 2006; 12: 342-347.
54. Pien GC, Basner-Tschakarjan, E, Hui, DJ, et al. Capsid antigen presentation flags human hepatocytes for destruction after transduction by adeno-associated viral vectors. J Clin Invest 2009; 119: 1688-95.
55. Nathwani AC, Gray, JT, Ng, CYC, et al. Self complementary adeno-associated virus vectors containing a novel liver-specific human factor IX expression cassette enable highly efficient transduction of murine and nonhuman primate liver Blood 2006; 107: 2653-2661.
56. Nathwani A, Tuddenham, E, Rosales, C, et al. Early Clinical Trial Results Following Administration of a Low Dose of a Novel Self Complementary Adeno-Associated Viral Vector Encoding Human Factor IX In Two Subjects with Severe Hemophilia B. Blood 2010; 116: A248.
57. Guilcher GM, Scully, MF, Harvey, M, Hand, JP. Treatment of intracranial and extracranial haemorrhages in a neonate with severe haemophilia B with recombinant factor IX infusion. Haemophilia 2005; 11: 411-4.
58. Pollmann H, Richter, H, Ringkamp, H, Jurgens, H. When are children diagnosed as having severe haemophilia and when do they start to bleed? A 10-year single-centre PUP study. Eur J Pediatr 1999; 158 Suppl 3: S166-70.
59. Santagostino E, Mancuso, ME. Prevention of arthropathy in haemophilia: prophylaxis. Haemophilia 2008; 14 Suppl 6: 16-9.
60. Mancuso ME, Graca, L, Auerswald, G, Santagostino, E. Haemophilia care in children--benefits of early prophylaxis for inhibitor prevention. Haemophilia 2009; 15 Suppl 1: 8-14.
61. Xu L, Gao, C, Sands, MS, et al. Neonatal or hepatocyte growth factor-potentiated adult gene therapy with a retroviral vector results in therapeutic levels of canine factor IX for hemophilia B. Blood 2003; 101: 3924-3932.
62. Zhang J, Xu, L, Haskins, ME, Ponder, KP. Neonatal gene transfer with a retroviral vector results in tolerance to human factor IX in mice and dogs. Blood 2004; 103: 143-51.
63. Xu L, Nichols, TC, Sarkar, R, et al. Absence of a desmopressin response after therapeutic expression of factor VIII in hemophilia A dogs with liver-directed neonatal gene therapy. Proc Natl Acad Sci USA 2005.
64. Xu L, Mei, M, Ma, X, Ponder, KP. High expression reduces an antibody response after neonatal gene therapy with B domaindeleted human factor VIII in mice. J Thromb Haemost 2007; 5: 1805-12.
65. VandenDriessche T, Vanslembrouck, V, Goovaerts, I, et al. Longterm expression of human coagulation factor VIII and correction of hemophilia A after in vivo retroviral gene transfer in factor VIIIdeficient mice. Proc Natl Acad Sci USA 1999; 96: 10379-84.
66. Waddington SN, Nivsarkar, M, Mistry, A, et al. Permanent phenotypic correction of Haemophilia B in immunocompetent mice by prenatal gene therapy. Blood 2004; 104: 2714-21.
67. Ward NJ, Buckley, SMK, Waddington, SN, et al. Codon optimisation of human factor VIII cDNAs leads to high level expression. Blood 2010; 117: 798-807.
68. Howe SJ, Mansour, MR, Schwarzwaelder, K, et al. Insertional mutagenesis combined with acquired somatic mutations causes leukemogenesis following gene therapy of SCID-X1 patients. J Clin Invest 2008; 118: 3143-3150.
69. Lipshutz GS, Sarkar, R, Flebbe-Rehwaldt, L, Kazazian, H, Gaensler, KM. 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 1999; 96: 13324-9.
70. Tuddenham EG, Ingerslev, J, Norengaard Sorensen, L, et al. Genetic aspects and research development in haemostasis. Haemophilia 2008; 14: 113-118.
71. Hu C, Cela, RG, Suzuki, M, Lee, B, Lipshutz, GS. Neonatal helperdependent adenoviral vector gene therapy mediates correction of hemophilia A and tolerance to human factor VIII. Proc Natl Acad Sci USA 2011; 108: 2082-2087.
72. Schneider H, Mühle, C, Douar, AM, et al. Sustained delivery of therapeutic concentrations of human clotting factor IX - a comparison of adenoviral and AAV vectors administered in utero. J. Gene Med. 2002; 4: 46-53.
73. Sabatino DE, Mackenzie, TC, Peranteau, W, et al. Persistent Expression of hF.IX After Tolerance Induction by In Utero or Neonatal Administration of AAV-1-F.IX in Hemophilia B Mice. Mol Ther 2007; 12: 12.
74. David AL, McIntosh, J, Peebles, DM, et al. Recombinant adenoassociated virus-mediated in utero gene transfer gives therapeutic transgene expression in the sheep. Hum Gene Ther 2010; 22: 419-426.
75. [Mattar CNZ, Nathwani, AC, Waddington, SN, et al. Stable human FIX expression after Intrauterine Gene Transfer of Selfcomplementary Adeno-Associated Viral Vector 5 and 8 in Macaques. Mol Ther 2011; In Press.
76. Menegatti M, Peyvandi, F. Factor X deficiency. Semin Thromb Hemost 2009; 35: 407-15.
77. Herrmann FH, Navarette, M, Salazar-Sanchez, L, et al. Homozygous Factor X gene mutations Gly380Arg and Tyr163delAT are associated with perinatal intracranial hemorrhage. J Pediatr 2005; 146: 128-30.
78. Le M, Okuyama, T, Cai, SR, et al. Therapeutic levels of functional human factor X in rats after retroviral-mediated hepatic gene therapy. Blood 1997; 89: 1254-9.
79. Xu L, Daly, T, Gao, C, et al. CMV-beta-Actin Promoter Directs Higher Expression from an Adeno- Associated Viral Vector in the Liver than the Cytomegalovirus or Elongation Factor 1alpha Promoter and Results in Therapeutic Levels of Human Factor X in Mice. Hum Gene Ther 2001; 12: 563-73.
80. McVey JH, Boswell, E, Mumford, AD, Kemball-Cook, G, Tuddenham, EG. Factor VII deficiency and the FVII mutation database. Hum Mutat 2001; 17: 3-17.
81. Peyvandi F, Kaufman, RJ, Seligsohn, U, et al. Rare bleeding disorders. Haemophilia 2006; 12 Suppl 3: 137-42.
82. Binny CJ, McIntosh, JH, Tuddenham, E, et al. Assessing the Potential of Perinatal Gene Transfer Using Congenital Factor VII Deficiency as a Model System. Blood 2010; 116: A247.
83. Loirat C, Veyradier, A, Girma, JP, Ribba, AS, Meyer, D. Thrombotic thrombocytopenic purpura associated with von Willebrand factor-cleaving protease (ADAMTS13) deficiency in children. Semin Thromb Hemost 2006; 32: 90-7.
84. Niiya M, Endo, M, Shang, D, et al. Correction of ADAMTS13 Deficiency by In Utero Gene Transfer of Lentiviral Vector encoding ADAMTS13 Genes. Mol Ther 2008; 17: 34-41.
85. Summar ML. In Pagon RA, Bird TD, Dolan CR, Stephens K, editors. GeneReviews [Internet]. Seattle (WA): University of Washington, Seattle; 1993-1993.
86. McBride KL, Miller, G, Carter, S, et al. Developmental outcomes with early orthotopic liver transplantation for infants with neonatalonset urea cycle defects and a female patient with late-onset ornithine transcarbamylase deficiency. Pediatrics 2004; 114: e523-6.
87. Ensenauer R, Tuchman, M, El-Youssef, M, et al. Management and outcome of neonatal-onset ornithine transcarbamylase deficiency following liver transplantation at 60 days of life. Mol Genet Metab 2005; 84: 363-6.
88. Filloux F, Townsend, JJ, Leonard, C. Ornithine transcarbamylase deficiency: neuropathologic changes acquired in utero. J Pediatr 1986; 108: 942-5.
89. Stratford-Perricaudet LD, Levrero, M, Chasse, JF, Perricaudet, M, Briand, P. Evaluation of the transfer and expression in mice of an enzyme-encoding gene using a human adenovirus vector. Hum Gene Ther 1990; 1: 241-56.
90. Morsy MA, Zhao, JZ, Ngo, TT, et al. Patient selection may affect gene therapy success. Dominant negative effects observed for ornithine transcarbamylase in mouse and human hepatocytes. J Clin Invest 1996; 97: 826-32.
91. Mian A, McCormack, WM, Jr., Mane, V, et al. Long-Term Correction of Ornithine Transcarbamylase Deficiency by WPREMediated Overexpression Using a Helper-Dependent Adenovirus. Mol Ther 2004; 10: 492-9.
92. Brunetti-Pierri N, Clarke, C, Mane, V, et al. Phenotypic correction of ornithine transcarbamylase deficiency using low dose helperdependent adenoviral vectors. J Gene Med 2008; 10: 890-6.
93. Moscioni D, Morizono, H, McCarter, RJ, et al. Long-term correction of ammonia metabolism and prolonged survival in ornithine transcarbamylase-deficient mice following liver-directed treatment with adeno-associated viral vectors. Mol Ther 2006; 14: 25-33.
94. Cunningham SC, Spinoulas, A, Carpenter, KH, et al. AAV2/8- mediated correction of OTC deficiency is robust in adult but not neonatal Spf(ash) mice. Mol Ther 2009; 17: 1340-6.
95. Gau CL, Rosenblatt, RA, Cerullo, V, et al. Short-term Correction of Arginase Deficiency in a Neonatal Murine Model With a Helper-dependent Adenoviral Vector. Mol Ther 2009; 17: 1155-1163.
96. Ye X, Whiteman, B, Jerebtsova, M, Batshaw, ML. Correction of argininosuccinate synthetase (AS) deficiency in a murine model of citrullinemia with recombinant adenovirus carrying human AS cDNA. Gene Ther 2000; 7: 1777-82.
97. Ogier de Baulny H, Saudubray, JM. Branched-chain organic acidurias. Semin Neonatol 2002; 7: 65-74.
98. Saudubray JM, Nassogne, MC, de Lonlay, P, Touati, G. Clinical approach to inherited metabolic disorders in neonates: an overview. Semin Neonatol 2002; 7: 3-15.
99. Seashore MR. In Pagon RA, Bird TD, Dolan CR, Stephens K, editors. GeneReviews [Internet]. Seattle (WA): University of Washington, Seattle; 1993-1993.
100. Homanics GE, Skvorak, K, Ferguson, C, Watkins, S, Paul, HS. Production and characterization of murine models of classic and intermediate maple syrup urine disease. BMC Med Genet 2006; 7: 33.
101. Chandler RJ, Chandrasekaran, S, Carrillo-Carrasco, N, et al. Adeno-Associated Virus Serotype 8 Gene Transfer Rescues a Neonatal Lethal Murine Model of Propionic Acidemia. Hum Gene Ther 2011; 22: 477-481.
102. Chandler RJ, Venditti, CP. Adenovirus-Mediated Gene Delivery Rescues a Neonatal Lethal Murine Model of mut(0) Methylmalonic Acidemia. Hum Gene Ther 2008; 19: 53-60.
103. Carrillo-Carrasco N, Chandler, RJ, Chandrasekaran, S, Venditti, CP. Liver-directed recombinant adeno-associated viral gene delivery rescues a lethal mouse model of methylmalonic acidemia and provides long-term phenotypic correction. Hum Gene Ther 2010; 21: 1147-54.
104. Hofherr S, Senac, JS, Chen, CY, et al. Short-term Rescue of Neonatal Lethality in a Mouse Model of Propionic Acidemia by Gene Therapy. Hum Gene Ther 2009; 20: 169-180.
105. Wraith JE. Lysosomal disorders. Semin Neonatol 2002; 7: 75-83.
106. Clarke LA. The mucopolysaccharidoses: a success of molecular medicine. Expert Rev Mol Med 2008; 10: e1.
107. Peters C, Shapiro, EG, Anderson, J, et al. Hurler syndrome: II. Outcome of HLA-genotypically identical sibling and HLAhaploidentical related donor bone marrow transplantation in fiftyfour children. The Storage Disease Collaborative Study Group. Blood 1998; 91: 2601-8.
108. Ponder KP, Haskins, ME. Gene therapy for mucopolysaccharidosis. Expert Opin Biol Ther 2007; 7: 1333-45.
109. Kamata Y, Tanabe, A, Kanaji, A, et al. Long-term normalization in the central nervous system, ocular manifestations, and skeletal deformities by a single systemic adenovirus injection into neonatal mice with mucopolysaccharidosis VII. Gene Ther 2003; 10: 406-14.
110. Kanaji A, Kosuga, M, Li, XK, et al. Improvement of skeletal lesions in mice with mucopolysaccharidosis type vii by neonatal adenoviral gene transfer. Mol Ther 2003; 8: 718-25.
111. Hartung SD, Frandsen, JL, Pan, D, et al. Correction of metabolic, craniofacial, and neurologic abnormalities in MPS I mice treated at birth with adeno-associated virus vector transducing the human alpha-L-iduronidase gene. Mol Ther 2004; 9: 866-75.
112. Donsante A, Levy, B, Vogler, C, Sands, MS. Clinical response to persistent, low-level beta-glucuronidase expression in the murine model of mucopolysaccharidosis type VII. J Inherit Metab Dis 2007; 30: 227-38.
113. Cardone M, Polito, VA, Pepe, S, et al. Correction of Hunter syndrome in the MPSII mouse model by AAV2/8-mediated gene delivery. Hum Mol Genet 2006; 15: 1225-36.
114. Tessitore A, Faella, A, O'Malley, T, et al. Biochemical, pathological, and skeletal improvement of mucopolysaccharidosis VI after gene transfer to liver but not to muscle. Mol Ther 2008; 16: 30-7.
115. Chung S, Ma, X, Liu, Y, et al. Effect of neonatal administration of a retroviral vector expressing alpha-l-iduronidase upon lysosomal storage in brain and other organs in mucopolysaccharidosis I mice. Mol Genet Metab 2007; 90: 181-192.
116. Liu Y, Xu, L, Hennig, AK, et al. Liver-directed neonatal gene therapy prevents cardiac, bone, ear, and eye disease in mucopolysaccharidosis I mice. Mol Ther 2005; 11: 35-47.
117. Ponder KP, Wang, B, Wang, P, et al. Mucopolysaccharidosis I cats mount a cytotoxic T lymphocyte response after neonatal gene therapy that can be blocked with CTLA4-Ig. Mol Ther 2006; 14: 5-13.
118. Meertens L, Zhao, Y, Rosic-Kablar, S, et al. In utero injection of alpha-L-iduronidase-carrying retrovirus in canine mucopolysaccharidosis type I: infection of multiple tissues and neonatal gene expression. Hum Gene Ther 2002; 13: 1809-20.
119. Traas AM, Wang, P, Ma, X, et al. Correction of clinical manifestations of canine mucopolysaccharidosis I with neonatal retroviral vector gene therapy. Mol Ther 2007; 15: 1423-31.
120. Xu L, Mango, RL, Sands, MS, et al. Evaluation of Pathological Manifestations of Disease in Mucopolysaccharidosis VII Mice after Neonatal Hepatic Gene Therapy. Mol Ther 2002; 6: 745-58.
121. Ponder KP, Melniczek, JR, Xu, L, et al. Therapeutic neonatal hepatic gene therapy in mucopolysaccharidosis VII dogs. Proc Natl Acad Sci USA 2002; 99: 13102-7.
122. Sleeper MM, Fornasari, B, Ellinwood, NM, et al. Gene therapy ameliorates cardiovascular disease in dogs with mucopolysaccharidosis VII. Circulation 2004; 110: 815-20.
123. Mango RL, Xu, L, Sands, MS, et al. Neonatal retroviral vectormediated hepatic gene therapy reduces bone, joint, and cartilage disease in mucopolysaccharidosis VII mice and dogs. Mol Genet Metab 2004; 82: 4-19.
124. Wang B, O'Malley T, M, Xu, L, et al. Expression in blood cells may contribute to biochemical and pathological improvements after neonatal intravenous gene therapy for mucopolysaccharidosis VII in dogs. Mol Genet Metab 2005.
125. Casal ML, Wolfe, JH. In utero transplantation of fetal liver cells in the mucopolysaccharidosis type VII mouse results in low-level chimerism, but overexpression of beta-glucuronidase can delay onset of clinical signs. Blood 2001; 97: 1625-1634.
126. Metcalf JA, Ma, X, Linders, B, et al. A Self-inactivating gamma- Retroviral Vector Reduces Manifestations of Mucopolysaccharidosis I in Mice. Mol Ther 2009; 18: 334-342.
127. Ogawa K, Hirai, Y, Ishizaki, M, et al. Long-term inhibition of glycosphingolipid accumulation in Fabry model mice by a single systemic injection of AAV1 vector in the neonatal period. Mol Genet Metab 2009; 96: 91-6.
128. Wolfsdorf JI, Weinstein, DA. Glycogen storage diseases. Rev Endocr Metab Disord 2003; 4: 95-102.
129. Ozen H. Glycogen storage diseases: new perspectives. World J Gastroenterol 2007; 13: 2541-53.
130. Koeberl DD, Kishnani, PS, Chen, YT. Glycogen storage disease types I and II: treatment updates. J Inherit Metab Dis 2007; 30: 159-64.
131. Zingone A, Hiraiwa, H, Pan, CJ, et al. Correction of glycogen storage disease type 1a in a mouse model by gene therapy. J Biol Chem 2000; 275: 828-32.
132. Somia N, Verma, IM. Gene therapy: trials and tribulations. Nat Rev Genet 2000; 1: 91-9.
133. Ghosh A, Allamarvdasht, M, Pan, CJ, et al. Long-term correction of murine glycogen storage disease type Ia by recombinant adenoassociated virus-1-mediated gene transfer. Gene Ther 2006; 13: 321-9.
134. Koeberl DD, Sun, BD, Damodaran, TV, et al. Early, sustained efficacy of adeno-associated virus vector-mediated gene therapy in glycogen storage disease type Ia. Gene Ther 2006; 13: 1430.
135. Koeberl DD, Pinto, C, Sun, B, et al. AAV vector-mediated reversal of hypoglycemia in canine and murine glycogen storage disease type Ia. Mol Ther 2008; 16: 665-72.
136. Weinstein DA, Correia, CE, Conlon, T, et al. AAV-Mediated Correction of a Canine Model of Glycogen Storage Disease Type Ia. Hum Gene Ther 2010.
137. Koeberl DD, Sun, B, Bird, A, et al. Efficacy of helper-dependent adenovirus vector-mediated gene therapy in murine glycogen storage disease type Ia. Mol Ther 2007; 15: 1253-8.
138. Di Mauro S. Muscle glycogenoses: an overview. Acta Myol 2007; 26: 35-41.
139. Watchko JF, Lin, Z. Exploring the genetic architecture of neonatal hyperbilirubinemia. Semin Fetal Neonatal Med 2010; 15: 169-75.
140. Strassburg CP. Hyperbilirubinemia syndromes (Gilbert- Meulengracht, Crigler-Najjar, Dubin-Johnson, and Rotor syndrome). Best Pract Res Clin Gastroenterol 2010; 24: 555-71.
141. Schauer R, Stangl, M, Lang, T, et al. Treatment of Crigler-Najjar type 1 disease: relevance of early liver transplantation. J Pediatr Surg 2003; 38: 1227-31.
142. Seppen J, van der Rijt, R, Looije, N, et al. Long-term correction of bilirubin UDPglucuronyltransferase deficiency in rats by in utero lentiviral gene transfer. Mol Ther 2003; 8: 593-9.
143. Seppen J, van Til, NP, van der Rijt, R, et al. Immune response to lentiviral bilirubin UDP-glucuronosyltransferase gene transfer in fetal and neonatal rats. Gene Ther 2006; 13: 672-677.
144. Matsui H, Hegadorn, C, Ozelo, M, et al. A MicroRNA-regulated and GP64-pseudotyped Lentiviral Vector Mediates Stable Expression of FVIII in a Murine Model of Hemophilia A. Mol Ther 2011; 19: 723-730.
145. Nguyen TH, Aubert, D, Bellodi-Privato, M, et al. Critical assessment of lifelong phenotype correction in hyperbilirubinemic Gunn rats after retroviral mediated gene transfer. Gene Ther 2007; 14: 1270-7.
146. Carbonaro DA, Jin, X, Petersen, D, et al. In vivo transduction by intravenous injection of a lentiviral vector expressing human ADA into neonatal ADA gene knockout mice: a novel form of enzyme replacement therapy for ADA deficiency. Mol Ther 2006; 13: 1110-20.
147. Spitzer D, Wu, X, Ma, X, et al. Cutting edge: treatment of complement regulatory protein deficiency by retroviral in vivo gene therapy. J Immunol 2006; 177: 4953-6.
148. Talbot GE, Waddington, SN, Bales, O, Tchen, RC, Antoniou, MN. Desmin-regulated Lentiviral Vectors for Skeletal Muscle Gene Transfer. Mol Ther 2010; 18: 601-608.
149. Tittiger M, Ma, X, Xu, L, Ponder, KP. Neonatal intravenous injection of a gammaretroviral vector has a low incidence of tumor induction in mice. Hum Gene Ther 2008; 19: 1317-23.
150. Donsante A, Vogler, C, Muzyczka, N, et al. Observed incidence of tumorigenesis in long-term rodent studies of rAAV vectors. Gene Ther 2001; 8: 1343-6.
151. Donsante A, Miller, DG, Li, Y, et al. AAV vector integration sites in mouse hepatocellular carcinoma. Science 2007; 317: 477.
152. Nathwani AC, Rosales, C, McIntosh, J, et al. Long-term safety and efficacy following systemic administration of a self-complementary AAV vector encoding human FIX pseudotyped with serotype 5 and 8 capsid proteins. Mol Ther 2011; 19: 876-885.
153. Flageul M, Aubert, D, Pichard, V, et al. Transient expression of genes delivered to newborn rat liver using recombinant adenoassociated virus 2/8 vectors. J Gene Med 2009; 11: 689-96.
154. Inagaki K, Piao, C, Kotchey, NM, Wu, X, Nakai, H. Frequency and spectrum of genomic integration of recombinant adeno-associated virus serotype 8 vector in neonatal mouse liver. J Virol 2008; 82: 9513-24.
155. Ponder KP. Immunology of neonatal gene transfer. Curr Gene Ther 2007; 7: 403-10.
156. Billingham RE, Brent, L, Medawar, PB. Actively acquired tolerance of foreign cells. Nature 1953; 172: 603-606.
157. Jiang H, van de Ven, C, Baxi, L, Satwani, P, Cairo, MS. Differential gene expression signatures of adult peripheral blood vs cord blood monocyte-derived immature and mature dendritic cells. Exp Hematol 2009; 37: 1201-15.
158. Goldenberg NA, Manco-Johnson, MJ. Protein C deficiency. Haemophilia 2008; 14: 1214-21.
159. Pollock-Barziv SM, McCrindle, BW, West, LJ, Dipchand, AI. Waiting before birth: outcomes after fetal listing for heart transplantation. Am J Transplant 2008; 8: 412-8.
160. Guo Y, Zhang, X, Huang, J, et al. Relationships between hematopoiesis and hepatogenesis in the midtrimester fetal liver characterized by dynamic transcriptomic and proteomic profiles. PLoS ONE 2009; 4: e7641.
161. Collardeau-Frachon S, Scoazec, JY. Vascular development and differentiation during human liver organogenesis. Anat Rec (Hoboken) 2008; 291: 614-27.
162. Hayes IM, Collins, V, Sahhar, M, Wraith, JE, Delatycki, MB. Newborn screening for mucopolysaccharidoses: opinions of patients and their families. Clin Genet 2007; 71: 446-50.
163. Bainbridge JW, Smith, AJ, Barker, SS, et al. Effect of Gene Therapy on Visual Function in Leber's Congenital Amaurosis. N Engl J Med 2008; 358: 2231-2239.
164. Maguire AM, Simonelli, F, Pierce, EA, et al. Safety and Efficacy of Gene Transfer for Leber's Congenital Amaurosis. N Engl J Med 2008; 358: 2240-2248.
165. Cideciyan AV, Hauswirth, WW, Aleman, TS, et al. Human RPE65 gene therapy for Leber congenital amaurosis: persistence of early visual improvements and safety at 1 year. Hum Gene Ther 2009; 20: 999-1004.
166. Hacein-Bey-Abina S, Le Deist, F, Carlier, F, et al. Sustained correction of X-linked severe combined immunodeficiency by ex vivo gene therapy. N Engl J Med 2002; 346: 1185-93.
167. Aiuti A, Slavin, S, Aker, M, et al. Correction of ADA-SCID by stem cell gene therapy combined with nonmyeloablative conditioning. Science 2002; 296: 2410-3.
168. Cartier N, Hacein-Bey-Abina, S, Bartholomae, CC, et al. Hematopoietic stem cell gene therapy with a lentiviral vector in Xlinked adrenoleukodystrophy. Science 2009; 326: 818-23.
169. Sheridan C. Gene therapy finds its niche. Nat Biotechnol 2011; 29: 121-8.
170. Cao H, Yang, T, Li, XF, et al. Readministration of helperdependent adenoviral vectors to mouse airway mediated via transient immunosuppression. Gene Ther 2011; 18: 173-81.
171. Phillips JB, Billson, VR, Forbes, AB. Autopsy standards for fetal lengths and organ weights of an Australian perinatal population. Pathology 2009; 41: 515-26.
172. Bolton-Maggs PH, Pasi, KJ. Haemophilias A and B. Lancet 2003; 361: 1801-9.
173. Hesiod. Theogony and Works and Days, Oxford Paperbacks 2008