Adeno-associated virus vector-based gene therapy for monogenetic metabolic diseases of the liver

Journal of Pediatric Gastroenterology and Nutrition

Volumn 60, Issue 4, 2015, Pages 433-440

  Junge, Norman ^a   Mingozzi, Federico ^b   Ott, Michael ^c   Baumann, Ulrich ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b GÉNÉTHON   (France)

^c INSTITUTE OF INFECTION IMMUNOLOGY   (Germany)

Author keywords

gene therapy; liver; metabolic; pediatric

Indexed keywords

LIPOSOME; NAKED DNA; NANOPARTICLE; PARVOVIRUS VECTOR; PLASMID DNA;

ACUTE INTERMITTENT PORPHYRIA; ARTICLE; CITRULLINEMIA; CLINICAL TRIAL (TOPIC); FAMILIAL HYPERCHOLESTEROLEMIA; GENE SILENCING; GENE TARGETING; GENOMICS; GENOTOXICITY; HEMOPHILIA B; HISTORY OF MEDICINE; HOMOLOGOUS RECOMBINATION; HORIZONTAL GENE TRANSFER; HUMAN; IMMUNOGENICITY; IMMUNOTOXICITY; IN VIVO GENE TRANSFER; INTRAHEPATIC CHOLESTASIS; LIVER DISEASE; LIVER TRANSPLANTATION; METABOLIC DISORDER; MORBIDITY; MORTALITY; NONHUMAN; ORNITHINE TRANSCARBAMYLASE DEFICIENCY; OXALOSIS 1; PATIENT SAFETY; PHENOTOXICITY; PRIORITY JOURNAL; PROGRESSIVE FAMILIAL INTRAHEPATIC CHOLESTASIS; PROPIONIC ACIDEMIA; QUALITY OF LIFE; TYROSINEMIA; VERTICAL TRANSMISSION; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; DEPENDOPARVOVIRUS; GENE THERAPY; GENE VECTOR; GENETICS; LIVER DISEASES; METABOLIC DISEASES; METABOLISM;

ADENO-ASSOCIATED VIRUS;

DEPENDOVIRUS; GENETIC THERAPY; GENETIC VECTORS; HUMANS; LIVER DISEASES; METABOLIC DISEASES;

EID: 84927176275     PISSN: 02772116     EISSN: 15364801     Source Type: Journal    
DOI: 10.1097/MPG.0000000000000703     Document Type: Article

References (83)

1. McCandless SE, Brunger JW, Cassidy SB. The burden of genetic disease on inpatient care in a children's hospital. Am J Hum Genet 2004;74:121-7.
2. Rosenberg SA, Aebersold P, Cornetta K, et al. Gene transfer into humans-immunotherapy of patients with advanced melanoma, using tumor-infiltrating lymphocytes modified by retroviral gene transduction. N Engl J Med 1990;323:570-8.
3. 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;80:148-58.
4. Cavazzana-Calvo M, Hacein-Bey S, de Saint Basile G, et al. Gene therapy of human severe combined immunodeficiency (SCID)-X1 disease. Science 2000;288:669-72.
5. Hacein-Bey-Abina S, Hauer J, Lim A, et al. Efficacy of gene therapy for X-linked severe combined immunodeficiency. N Engl J Med 2010;363:355-64.
6. 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.
7. Naldini L. Ex vivo gene transfer and correction for cell-based therapies. Nat Rev Genet 2011;12:301-15.
8. Aiuti A, Biasco L, Scaramuzza S, et al. Lentiviral hematopoietic stem cell gene therapy in patients with Wiskott-Aldrich syndrome. Science 2013;341:1233151.
9. 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;326:818-23.
10. Biffi A, Montini E, Lorioli L, et al. Lentiviral hematopoietic stem cell gene therapy benefits metachromatic leukodystrophy. Science 2013; 341:1233158.
11. Cavazzana-Calvo M, Payen E, Negre O, et al. Transfusion independence and HMGA2 activation after gene therapy of human beta-thalassaemia. Nature 2010;467:318-22.
12. 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;358:2231-9.
13. Cideciyan AV, Aleman TS, Boye SL, et al. Human gene therapy for RPE65 isomerase deficiency activates the retinoid cycle of vision but with slow rod kinetics. Proc Natl Acad Sci U S A 2008;105: 15112-7.
14. 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: 2240-8.
15. Nathwani AC, Tuddenham EG, Rangarajan S, et al. Adenovirus-associated virus vector-mediated gene transfer in hemophilia B. N Engl J Med 2011;365:2357-65.
16. Manno CS, Pierce GF, Arruda VR, et al. Successful transduction of liver in hemophilia by AAV-factor IX and limitations imposed by the host immune response. Nat Med 2006;12:342-7.
17. Kaufmann KB, Buning H, Galy A, et al. Gene therapy on the move. EMBO Mol Med 2013;5:1642-61.
18. Li H, Malani N, Hamilton SR, et al. Assessing the potential for AAV vector genotoxicity in a murine model. Blood 2011;117:3311-9.
19. Li H, Haurigot V, Doyon Y, et al. In vivo genome editing restores haemostasis in a mouse model of haemophilia. Nature 2011;475:217-21.
20. 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.
21. Sawyer GJ, Rela M, Davenport M, et al. Hydrodynamic gene delivery to the liver: theoretical and practical issues for clinical application. Curr Gene Ther 2009;9:128-35.
22. Lungwitz U, Breunig M, Blunk T, et al. Polyethylenimine-based nonviral gene delivery systems. Eur J Pharm Biopharm 2005;60:247-66.
23. Mingozzi F, High KA. Therapeutic in vivo gene transfer for genetic disease using AAV: progress and challenges. Nat Rev Genet 2011; 12:341-55.
24. Tebas P, Stein D, Tang WW, et al. Gene editing of CCR5 in autologous CD4 T cells of persons infected with HIV. N Engl J Med 2014;370:901-10.
25. Inagaki K, Piao C, Kotchey NM, et al. Frequency and spectrum of genomic integration of recombinant adeno-associated virus serotype 8 vector in neonatal mouse liver. J Virol 2008;82:9513-24.
26. Donsante A, Miller DG, Li Y, et al. AAV vector integration sites in mouse hepatocellular carcinoma. Science 2007;317:477.
27. 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.
28. 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;19:876-85.
29. Li H, Malani N, Hamilton SR, et al. Assessing the potential for AAV vector genotoxicity in a murine model. Blood 2011; 117:3311-9.
30. 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.
31. Wellman JA, Mingozzi F, Ozelo MC, et al. Results from the long-term follow-up of severe hemophilia B subjects previously enrolled in a clinical study of AAV2-FIX gene transfer to the liver. Mol Ther 2012;20:28-9.
32. Jiang H, Couto LB, Patarroyo-White S, et al. Effects of transient immunosuppression on adenoassociated, virus-mediated, liver-directed gene transfer in rhesus macaques and implications for human gene therapy. Blood 2006;108:3321-8.
33. Scallan CD, Jiang H, Liu T, et al. Human immunoglobulin inhibits liver transduction by AAV vectors at low AAV2 neutralizing titers in SCID mice. Blood 2006;107:1810-7.
34. Calcedo R, Vandenberghe LH, Gao G, et al.Worldwide epidemiology of neutralizing antibodies to adeno-associated viruses. J Infect Dis 2009;199:381-90.
35. Calcedo R, Morizono H,Wang L, et al. Adeno-associated virus antibody profiles in newborns, children, and adolescents. Clin Vaccine Immunol 2011;18:1586-8.
36. Li C, Narkbunnam N, Samulski RJ, et al. Neutralizing antibodies against adeno-associated virus examined prospectively in pediatric patients with hemophilia. Gene Ther 2012;19:288-94.
37. Masat E, Pavani G, Mingozzi F. Humoral immunity to AAV vectors in gene therapy: challenges and potential solutions. Discov Med 2013;15: 379-89.
38. Mingozzi F, Anguela XM, Pavani G, et al. Overcoming preexisting humoral immunity to AAV using capsid decoys. Sci Transl Med 2013;5:194ra92.
39. Mingozzi F, Maus MV, Hui DJ, et al. CD8(+) T-cell responses to adenoassociated virus capsid in humans. Nat Med 2007;13:419-22.
40. Vandenberghe LH, Wang L, Somanathan S, et al. Heparin binding directs activation of T cells against adeno-associated virus serotype 2 capsid. Nat Med 2006;12:967-71.
41. Mingozzi F, Meulenberg JJ, Hui DJ, et al. AAV-1-mediated gene transfer to skeletal muscle in humans results in dose-dependent activation of capsid-specific T cells. Blood 2009;114:2077-86.
42. Montenegro-Miranda PS, ten Bloemendaal L, Kunne C, et al. Mycophenolate mofetil impairs transduction of single-stranded adeno-associated viral vectors. Hum Gene Ther 2011;22:605-12.
43. Unzu C, Hervas-Stubbs S, Sampedro A, et al. Transient and intensive pharmacological immunosuppression fails to improve AAV-based liver gene transfer in non-human primates. J Transl Med 2012;10: 122.
44. Finn JD, Hui D, Downey HD, et al. Proteasome inhibitors decrease AAV2 capsid derived peptide epitope presentation on MHC class I following transduction. Mol Ther 2010;18:135-42.
45. Martino AT, Basner-Tschakarjan E, Markusic DM, et al. Engineered AAV vector minimizes in vivo targeting of transduced hepatocytes by capsid-specific CD8+ T cells. Blood 2013;121:2224-33.
46. Hui DJ, Basner-Tschakarjan E, Chen Y, et al. Modulation of CD8+ T cell responses to AAV vectors with IgG-derived MHC class II epitopes. Mol Ther 2013;21:1727-37.
47. Mingozzi F, Liu YL, Dobrzynski E, et al. Induction of immune tolerance to coagulation factor IX antigen by in vivo hepatic gene transfer. J Clin Invest 2003;111:1347-56.
48. Rogers GL, Martino AT, Aslanidi GV, et al. Innate immune responses to AAV vectors. Front Microbiol 2011;2:194.
49. Wu T, Topfer K, Lin SW, et al. Self-complementary AAVs induce more potent transgene product-specific immune responses compared to a single-stranded genome. Mol Ther 2012;20:572-9.
50. Manno CS, Pierce GF, Arruda VR, et al. Successful transduction of liver in hemophilia by AAV-factor IX and limitations imposed by the host immune response. Nat Med 2006;12:342-7.
51. Favre D, Provost N, Blouin V, et al. Immediate and long-term safety of recombinant adeno-associated virus injection into the nonhuman primate muscle. Mol Ther 2001;4:559-66.
52. Arruda VR, Fields PA, Milner R, et al. Lack of germline transmission of vector sequences following systemic administration of recombinant AAV-2 vector in males. Mol Ther 2001;4:586-92.
53. Schuettrumpf J, Liu JH, Couto LB, et al. Inadvertent germline transmission of AAV2 vector: findings in a rabbit model correlate with those in a human clinical trial. Mol Ther 2006;13:1064-73.
54. Favaro P, Downey HD, Zhou JS, et al. Host and vector-dependent effects on the risk of germline transmission of AAV vectors. Mol Ther 2009;17:1022-30.
55. Nathwani AC, Gray JT, McIntosh J, et al. Safe and efficient transduction of the liver after peripheral vein infusion of self-complementary AAV vector results in stable therapeutic expression of human FIX in nonhuman primates. Blood 2007;109:1414-21.
56. Nathwani AC, Gray JT, Ng CY, et al. Self-complementary adenoassociated virus vectors containing a novel liver-specific human factor IX expression cassette enable highly efficient transduction of murine and nonhuman primate liver. Blood 2006;107:2653-61.
57. Finn JD, Nichols TC, Svoronos N, et al. The efficacy and the risk of immunogenicity of FIX Padua (R338L) in hemophilia B dogs treated by AAV muscle gene therapy. Blood 2012;120:4521-3.
58. Chuah MK, Petrus I, De Bleser P, et al. Liver-specific transcriptional modules identified by genome-wide in silico analysis enable efficient gene therapy in mice and non-human primates. Mol Ther 2014;22: 1605-13.
59. Gao GP, Alvira MR,Wang L, et al. Novel adeno-associated viruses from rhesus monkeys as vectors for human gene therapy. Proc Natl Acad Sci U S A 2002;99:11854-9.
60. 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.
61. Lisowski L, Dane AP, Chu K, et al. Selection and evaluation of clinically relevant AAV variants in a xenograft liver model. Nature 2014;506: 382-6.
62. Gao GP, Alvira MR,Wang L, et al. Novel adeno-associated viruses from rhesus monkeys as vectors for human gene therapy. Proc Natl Acad Sci U S A 2002;99:11854-9.
63. Gunn CH. Hereditary acholuric jaundice in a new mutant strain of rats. J Hered 1938;29:137-9.
64. Bortolussi G, Zentilin L, Baj G, et al. Rescue of bilirubin-induced neonatal lethality in a mouse model of Crigler-Najjar syndrome type I by AAV9-mediated gene transfer. FASEB J 2012;26:1052-63.
65. Fox IJ, Chowdhury JR, Kaufman SS, et al. Treatment of the Crigler-Najjar syndrome type I with hepatocyte transplantation. N Engl J Med 1998;338:1422-6.
66. Seppen J, Bakker C, de Jong B, et al. Adeno-associated virus vector serotypes mediate sustained correction of bilirubin UDP glucuronosyltransferase deficiency in rats. Mol Ther 2006;13:1085-92.
67. Collaud F, Ronzitti G, Lacoste F, et al. An optimized AAV vector for liver-directed expression of the UGT1A1 gene in Crigler-Najjar syndrome, towards clinical development. Mol Ther 2014;22:110.
68. Luo X, Hall G, Li S, et al. Hepatorenal correction in murine glycogen storage disease type I with a double-stranded adeno-associated virus vector. Mol Ther 2011;19:1961-70.
69. Lee YM, Jun HS, Pan CJ, et al. Prevention of hepatocellular adenoma and correction of metabolic abnormalities in murine glycogen storage disease type Ia by gene therapy. Hepatology 2012;56:1719-29.
70. Koeberl DD. In search of proof-of-concept: gene therapy for glycogen storage disease type Ia. J Inherit Metab Dis 2012;35:671-8.
71. Li H, Haurigot V, Doyon Y, et al. In vivo genome editing restores haemostasis in a mouse model of haemophilia. Nature 2011;475:217-21.
72. 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.
73. Chandler RJ, Chandrasekaran S, Carrillo-Carrasco N, et al. Adenoassociated virus serotype 8 gene transfer rescues a neonatal lethal murine model of propionic acidemia. Hum Gene Ther 2011;22:477-81.
74. 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;19:870-5.
75. Chandler RJ, Tarasenko TN, Cusmano-Ozog K, et al. Liver-directed adeno-associated virus serotype 8 gene transfer rescues a lethal murine model of citrullinemia type 1. Gene Ther 2013;20:1188-91.
76. Ye X, Robinson MB, Batshaw ML, et al. Prolonged metabolic correction in adult ornithine transcarbamylase-deficient mice with adenoviral vectors. J Biol Chem 1996;271:3639-46.
77. Alexander IE, Kok C, Dane AP, et al. Gene therapy for metabolic disorders: an overview with a focus on urea cycle disorders. J Inherit Metab Dis 2012;35:641-5.
78. Cunningham SC, Kok CY, Spinoulas A, et al. AAV-encoded OTC activity persisting to adulthood following delivery to newborn spf(ash) mice is insufficient to prevent shRNA-induced hyperammonaemia. Gene Ther 2013;20:1184-7.
79. Siew SM, Cunningham SC, Alexander IE. Neonatal treatment using a novel, hybrid recombinant AAVPIGGYBAC transposon vector results in robust, long-term phenotype correction of the progressive familial intrahepatic cholestasis type 3 mouse model in vivo. ESPGHAN. Hepatology 2014 [abstract no. SP-H-0157].
80. Unzu C, Sampedro A, Mauleon I, et al. Sustained enzymatic correction by rAAV-mediated liver gene therapy protects against induced motor neuropathy in acute porphyria mice. Mol Ther 2011;19:243-50.
81. Paneda A, Lopez-Franco E, Kaeppel C, et al. Safety and liver transduction efficacy of rAAV5-cohPBGD in nonhuman primates: a potential therapy for acute intermittent porphyria. Hum Gene Ther 2013;24:1007-17.
82. D'Avola D, Lopez-Franco E, Harper P, et al. Phase 1 clinical trial of liver directed gene therapy with rAAV5-PBGD in acute intermittent porphyria: preliminary safety data. Mol Ther 2014;22(Suppl 1):S7.
83. Hofherr SE, Matern D. Systematic ranking of inborn errors of metabolism as targets for gene therapy. Mol Genet Metab 2010;100:215-8.