Gene therapy for inherited diseases of liver metabolism

Human Gene Therapy

Volumn 26, Issue 4, 2015, Pages 186-192

  Piccolo, Pasquale ^a   Brunetti Pierri, Nicola ^a,b  

^a TELETHON INSTITUTE OF GENETICS AND MEDICINE TIGEM   (Italy)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA 1 ANTITRYPSIN; ANTISENSE OLIGONUCLEOTIDE; BLOOD CLOTTING FACTOR 9; CAPSID PROTEIN; LIVER ENZYME; LOW DENSITY LIPOPROTEIN RECEPTOR; LYSOSOME ENZYME; MICROSOMAL TRIGLYCERIDE TRANSFER PROTEIN INHIBITOR; MIPOMERSEN; ORNITHINE CARBAMOYLTRANSFERASE;

ACUTE INTERMITTENT PORPHYRIA; ALPHA 1 ANTITRYPSIN DEFICIENCY; CRIGLER NAJJAR SYNDROME; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME DEFICIENCY; ENZYME REPLACEMENT; EX VIVO GENE TRANSFER; FAMILIAL HYPERCHOLESTEROLEMIA; FATTY ACID OXIDATION; FATTY ACID OXIDATION DEFECT; GENE EXPRESSION; GENE REPLACEMENT THERAPY; GENE THERAPY; GENETIC DISORDER; GLYCOGEN STORAGE DISEASE TYPE 1; GLYCOGEN STORAGE DISEASE TYPE 3; GLYCOGEN STORAGE DISEASE TYPE 4; HUMAN; INHERITED DISEASE OF LIVER METABOLISM; INTRAHEPATIC CHOLESTASIS; LIVER DISEASE; LIVER TRANSPLANTATION; LYSOSOME STORAGE DISEASE; MAPLE SYRUP URINE DISEASE; METHYLMALONIC ACIDEMIA; NONHUMAN; ORNITHINE TRANSCARBAMYLASE DEFICIENCY; OXALOSIS 1; PROPIONIC ACIDEMIA; REVIEW; SEVERE COMBINED IMMUNODEFICIENCY; TYROSINEMIA; UREA CYCLE DISORDER; WILSON DISEASE; WISKOTT ALDRICH SYNDROME; ANIMAL; CLINICAL TRIAL (TOPIC); GENE VECTOR; GENETICS; LIVER DISEASES; METABOLIC DISEASES;

ANIMALS; CLINICAL TRIALS AS TOPIC; GENETIC THERAPY; GENETIC VECTORS; HUMANS; LIVER DISEASES; METABOLIC DISEASES;

EID: 84928503263     PISSN: 10430342     EISSN: 15577422     Source Type: Journal    
DOI: 10.1089/hum.2015.029     Document Type: Review

References (85)

1. Terheggen HG, Lowenthal A, Lavinha F, et al. Unsuccessful trial of gene replacement in arginase deficiency. Z Kinderheilkd 1975;119:1-3.
2. Miller AD, Eckner RJ, Jolly DJ, et al. Expression of a retrovirus encoding human HPRT in mice. Science 1984; 225:630-632.
3. Applegarth DA, Toone JR, Lowry RB. Incidence of inborn errors of metabolism in British Columbia, 1969-1996. Pediatrics 2000;105:e10.
4. Sanderson S, Green A, Preece MA, et al. The incidence of inherited metabolic disorders in the West Midlands, UK. Arch Dis Child 2006;91:896-899.
5. Levy HL. Newborn screening conditions: what we know, what we do not know, and how we will know it. Genet Med 2010;12:S213-S214.
6. Mazariegos G, Shneider B, Burton B, et al. Liver transplantation for pediatric metabolic disease. Mol Genet Metab 2014;111:418-427.
7. Teckman J, Perlmutter DH. Conceptual advances in the pathogenesis and treatment of childhood metabolic liver disease. Gastroenterology 1995;108:1263-1279.
8. Toso C, Ris F, Mentha G, et al. Potential impact of in situ liver splitting on the number of available grafts. Transplantation 2002;74:222-226.
9. Newstead CG. Assessment of risk of cancer after renal transplantation. Lancet 1998;351:610-611.
10. Shneider BL. Pediatric liver transplantation in metabolic disease: clinical decision making. Pediatr Transplant 2002;6:25-29.
11. Raper SE, Chirmule N, Lee FS, et al. Fatal systemic inflammatory response syndrome in a ornithine transcarbamylase deficient patient following adenoviral gene transfer. Mol Genet Metab 2003;80:148-158.
12. Wilson JM. Lessons learned from the gene therapy trial for ornithine transcarbamylase deficiency. Mol Genet Metab 2009;96:151-157.
13. Hacein-Bey-Abina S, Von Kalle C, Schmidt M, et al. LMO2- associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science 2003;302:415-419.
14. Braun CJ, Boztug K, Paruzynski A, et al. Gene therapy for Wiskott-Aldrich syndrome-long-term efficacy and genotoxicity. Sci Transl Med 2014;6:227ra33.
15. Raper SE, Yudkoff M, Chirmule N, et al. A pilot study of in vivo liver-directed gene transfer with an adenoviral vector in partial ornithine transcarbamylase deficiency. Hum Gene Ther 2002;13:163-175.
16. Brunetti-Pierri N, Palmer DJ, Beaudet AL, et al. Acute toxicity after high-dose systemic injection of helper-dependentadenoviral vectors into nonhuman primates. Hum Gene Ther 2004;15:35-46.
17. Muruve DA, Barnes MJ, Stillman IE, et al. Adenoviral gene therapy leads to rapid induction of multiple chemokines and acute neutrophil-dependent hepatic injury in vivo. Hum Gene Ther 1999;10:965-976.
18. Nathwani AC, Tuddenham EG, Rangarajan S, et al. Adenovirus-associated virus vector-mediated gene transfer in hemophilia B. N Engl J Med 2011;365:2357-2365.
19. Nathwani AC, Reiss UM, Tuddenham EG, et al. Long-term safety and efficacy of factor IX gene therapy in hemophilia B. N Engl J Med 2014;371:1994-2004.
20. Gonzalez-Aseguinolaza G. Augmenting PBGD expression in the liver as a novel gene therapy for acute intermittent porphyria (AIPgene). Hum Gene Ther Clin Dev 2014;25:61-63.
21. Brunetti-Pierri N, Liou A, Patel P, et al. Balloon catheter delivery of helper-dependent adenoviral vector results in sustained, therapeutic hFIX expression in rhesus macaques. Mol Ther 2012;20:1863-1870.
22. Brunetti-Pierri N, Ng T, Iannitti D, et al. Transgene expression up to 7 years in nonhuman primates following hepatic transduction with helper-dependent adenoviral vectors. Hum Gene Ther 2013;24:761-765.
23. Brunetti-Pierri N, Ng P. Helper-dependent adenoviral vectors for liver-directed gene therapy. Hum Mol Genet 2011;20:R7-R13.
24. SmithCA,Woodruff LS,KitchingmanGR, et al. Adenoviruspulsed dendritic cells stimulate human virus-specific T-cell responses in vitro. J Virol 1996;70:6733-6740.
25. Molinier-Frenkel V, Gahery-Segard H, Mehtali M, et al. Immune response to recombinant adenovirus in humans: capsid components from viral input are targets for vector-specific cytotoxic T lymphocytes. J Virol 2000;74:7678-7682.
26. Wang L, Figueredo J, Calcedo R, et al. Cross-presentation of adeno-associated virus serotype 2 capsids activates cytotoxic T cells but does not render hepatocytes effective cytolytic targets. Hum Gene Ther 2007;18:185-194.
27. Li H, Murphy SL, Giles-Davis W, et al. Pre-existing AAV capsid-specific CD8 + T cells are unable to eliminate AAVtransduced hepatocytes. Mol Ther 2007;15:792-800.
28. Li H, Lin SW, Giles-Davis W, et al. A preclinical animal model to assess the effect of pre-existing immunity on AAVmediated gene transfer. Mol Ther 2009;17:1215-1224.
29. Eastman SJ, Baskin KM, Hodges BL, et al. Development of catheter-based procedures for transducing the isolated rabbit liver with plasmid DNA. Hum Gene Ther 2002;13:2065-2077.
30. Alino SF, Herrero MJ, Noguera I, et al. Pig liver gene therapy by noninvasive interventionist catheterism. Gene Ther 2007;14:334-343.
31. Aiuti A, Cattaneo F, Galimberti S, et al. Gene therapy for immunodeficiency due to adenosine deaminase deficiency. N Engl J Med 2009;360:447-458.
32. 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;346:1185-1193.
33. Biffi A, Montini E, Lorioli L, et al. Lentiviral hematopoietic stem cell gene therapy benefits metachromatic leukodystrophy. Science 2013;341:1233158.
34. Cartier N, Hacein-Bey-Abina S, Bartholomae CC, et al. Hematopoietic stem cell gene therapy with a lentiviral vector in X-linked adrenoleukodystrophy. Science 2009;326:818-823.
35. Grossman M, Raper SE, Kozarsky K, et al. Successful ex vivo gene therapy directed to liver in a patient with familial hypercholesterolaemia. Nat Genet 1994;6:335-341.
36. Wisse E, Jacobs F, Topal B, et al. The size of endothelial fenestrae in human liver sinusoids: implications for hepatocytedirected gene transfer. Gene Ther 2008;15:1193-1199.
37. Brunetti-Pierri N, Palmer DJ, Mane V, et al. Increased hepatic transduction with reduced systemic dissemination and proinflammatory cytokines following hydrodynamic injection of helper-dependent adenoviral vectors. Mol Ther 2005;12:99-106.
38. Lievens J, Snoeys J, Vekemans K, et al. The size of sinusoidal fenestrae is a critical determinant of hepatocyte transduction after adenoviral gene transfer. Gene Ther 2004;11:1523-1531.
39. Snoeys J, Lievens J, Wisse E, et al. Species differences in transgene DNA uptake in hepatocytes after adenoviral transfer correlate with the size of endothelial fenestrae. Gene Ther 2007;14:604-612.
40. Van Dijk R, Montenegro-Miranda PS, Riviere C, et al. Polyinosinic acid blocks adeno-associated virus macrophage endocytosis in vitro and enhances adeno-associated virus liver-directed gene therapy in vivo. Hum Gene Ther 2013;24: 807-813.
41. Tao N, Gao GP, Parr M, et al. Sequestration of adenoviral vector by Kupffer cells leads to a nonlinear dose response of transduction in liver. Mol Ther 2001;3:28-35.
42. Ghosh A, Allamarvdasht M, Pan CJ, et al. Long-term correction of murine glycogen storage disease type Ia by recombinant adeno-associated virus-1-mediated gene transfer. Gene Ther 2006;13:321-329.
43. Merritt JL 2nd, Nguyen T, Daniels J, et al. Biochemical correction of very long-chain acyl-CoA dehydrogenase deficiency following adeno-associated virus gene therapy. Mol Ther 2009;17:425-429.
44. Nyhan WL, Gargus JJ, Boyle K, et al. Progressive neurologic disability in methylmalonic acidemia despite transplantation of the liver. Eur J Pediatr 2002;161:377-379.
45. Meyburg J, Hoffmann GF. Liver transplantation for inborn errors of metabolism. Transplantation 2005;80:S135-S137.
46. Mckiernan P. Liver transplantation and cell therapies for inborn errors of metabolism. J Inherit Metab Dis 2013;36: 675-680.
47. Fagiuoli S, Daina E, D'Antiga L, et al. Monogenic diseases that can be cured by liver transplantation. J Hepatol 2013; 59:595-612.
48. Brunetti-Pierri N, Lee B. Gene therapy for inborn errors of liver metabolism. Mol Genet Metab 2005;86:13-24.
49. Cotugno G, Annunziata P, Tessitore A, et al. Long-term amelioration of feline Mucopolysaccharidosis VI after AAVmediated liver gene transfer. Mol Ther 2011;19:461-469.
50. Hinderer C, Bell P, Gurda BL, et al. Liver-directed gene therapy corrects cardiovascular lesions in feline mucopolysaccharidosis type I. Proc Natl Acad Sci USA 2014;111: 14894-14899.
51. Batshaw ML, Tuchman M, Summar M, et al. A longitudinal study of urea cycle disorders. Mol Genet Metab 2014; 113:127-130.
52. 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.
53. Cunningham SC, Kok CY, Dane AP, et al. Induction and prevention of severe hyperammonemia in the spfash mouse model of ornithine transcarbamylase deficiency using shRNA and rAAV-mediated gene delivery. Mol Ther 2011;19:854-859.
54. Kok CY, Cunningham SC, Carpenter KH, et al. Adenoassociated virus-mediated rescue of neonatal lethality in argininosuccinate synthetase-deficient mice. Mol Ther 2013;21:1823-1831.
55. Wang L, Bell P, Lin J, et al. AAV8-mediated hepatic gene transfer in infant rhesus monkeys (Macaca mulatta). Mol Ther 2011;19:2012-2020.
56. Coppoletta JM, Wolbach SB. Body length and organ weights of infants and children: a study of the body length and normal weights of the more important vital organs of the body between birth and twelve years of age. Am J Pathol 1933;9:55-70.
57. Chandler RJ, Lafave MC, Varshney GK, et al. Vector design influences hepatic genotoxicity after adeno-associated virus gene therapy. J Clin Invest 2015;125:870-880.
58. Donsante A, Miller DG, Li Y, et al. AAV vector integration sites in mouse hepatocellular carcinoma. Science 2007;317: 477.
59. Li H, Malani N, Hamilton SR, et al. Assessing the potential for AAV vector genotoxicity in a murine model. Blood 2011;117:3311-3319.
60. Niemeyer GP, Herzog RW, Mount J, et al. Long-term correction of inhibitor-prone hemophilia B dogs treated with liver-directed AAV2-mediated factor IX gene therapy. Blood 2009;113:797-806.
61. Nathwani AC, Rosales C, Mcintosh J, et al. Long-term safety and efficacy following systemic administration of a selfcomplementary AAV vector encoding human FIX pseudotyped with serotype 5 and 8 capsid proteins. Mol Ther 2011; 19:876-885.
62. Strauss KA, Robinson DL, Vreman HJ, et al. Management of hyperbilirubinemia and prevention of kernicterus in 20 patients with Crigler-Najjar disease. Eur J Pediatr 2006; 165:306-319.
63. Fox IJ, Chowdhury JR, Kaufman SS, et al. Treatment of the Crigler-Najjar syndrome type I with hepatocyte transplantation. N Engl J Med 1998;338:1422-1426.
64. Pastore N, Nusco E, Piccolo P, et al. Improved efficacy and reduced toxicity by ultrasound-guided intrahepatic injections of helper-dependent adenoviral vector in Gunn rats. Hum Gene Ther Methods 2013;24:321-327.
65. Chowdhury JR, Kondapalli R, Chowdhury NR. Gunn rat: a model for inherited deficiency of bilirubin glucuronidation. Adv Vet Sci Comp Med 1993;37:149-173.
66. Bortolussi G, Zentilin L, Baj G, et al. Rescue of bilirubininduced neonatal lethality in a mouse model of Crigler- Najjar syndrome type I by AAV9-mediated gene transfer. FASEB J 2012;26:1052-1063.
67. Miranda PS, Bosma PJ. Towards liver-directed gene therapy for Crigler-Najjar syndrome. Curr Gene Ther 2009;9:72-82.
68. Bortolussi G, Zentillin L, Vanikova J, et al. Life-long correction of hyperbilirubinemia with a neonatal liver-specific AAV-mediated gene transfer in a lethal mouse model of Crigler-Najjar Syndrome. Hum Gene Ther 2014;25:844-855.
69. Montenegro-Miranda PS, Paneda A, Ten Bloemendaal L, et al. Adeno-associated viral vector serotype 5 poorly transduces liver in rat models. PLoS One 2013;8:e82597.
70. Widhalm K, Binder CB, Kreissl A, et al. Sudden death in a 4-year-old boy: a near-complete occlusion of the coronary artery caused by an aggressive low-density lipoprotein receptor mutation (W556R) in homozygous familial hypercholesterolemia. J Pediatr 2011;158:167.
71. Sniderman AD, Tsimikas S, Fazio S. The severe hypercholesterolemia phenotype: clinical diagnosis, management, and emerging therapies. J Am Coll Cardiol 2014;63:1935-1947.
72. Lebherz C, Gao G, Louboutin JP, et al. Gene therapy with novel adeno-associated virus vectors substantially diminishes atherosclerosis in a murine model of familial hypercholesterolemia. J Gene Med 2004;6:663-672.
73. Kassim SH, Li H, Bell P, et al. Adeno-associated virus serotype 8 gene therapy leads to significant lowering of plasma cholesterol levels in humanized mouse models of homozygous and heterozygous familial hypercholesterolemia. Hum Gene Ther 2013;24:19-26.
74. Chen SJ, Sanmiguel J, Lock M, et al. Biodistribution of AAV8 vectors expressing human low-density lipoprotein receptor in a mouse model of homozygous familial hypercholesterolemia. Hum Gene Ther Clin Dev 2013;24:154-160.
75. Cuchel M, Meagher EA, Du Toit Theron H, et al. Efficacy and safety of a microsomal triglyceride transfer protein inhibitor in patients with homozygous familial hypercholesterolaemia: a single-arm, open-label, phase 3 study. Lancet 2013;381:40-46.
76. Raal FJ, Santos RD, Blom DJ, et al. Mipomersen, an apolipoprotein B synthesis inhibitor, for lowering of LDL cholesterol concentrations in patients with homozygous familial hypercholesterolaemia: a randomised, doubleblind, placebo-controlled trial. Lancet 2010;375:998-1006.
77. Leumann E, Hoppe B. The primary hyperoxalurias. J Am Soc Nephrol 2001;12:1986-1993.
78. Hoppe B, Langman CB. A United States survey on diagnosis, treatment, and outcome of primary hyperoxaluria. Pediatr Nephrol 2003;18:986-991.
79. Cochat P, Koch Nogueira PC, Mahmoud MA, et al. Primary hyperoxaluria in infants: medical, ethical, and economic issues. J Pediatr 1999;135:746-750.
80. Millan MT, Berquist WE, So SK, et al. One hundred percent patient and kidney allograft survival with simultaneous liver and kidney transplantation in infants with primary hyperoxaluria: a single-center experience. Transplantation 2003;76: 1458-1463.
81. Cochat P, Faure JL, Divry P, et al. Liver transplantation in primary hyperoxaluria type 1. Lancet 1989;1:1142-1143.
82. Watts RW, Calne RY, Rolles K, et al. Successful treatment of primary hyperoxaluria type I by combined hepatic and renal transplantation. Lancet 1987;2:474-475.
83. Salido E, Rodriguez-Pena M, Santana A, et al. Phenotypic correction of a mouse model for primary hyperoxaluria with adeno-associated virus gene transfer. Mol Ther 2011; 19:870-875.
84. 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.
85. Yin H, Xue W, Chen S, et al. Genome editing with Cas9 in adult mice corrects a disease mutation and phenotype. Nat Biotechnol 2014;32:551-553.