Impact of age at administration, lysosomal storage, and transgene regulatory elements on AAV2/8-mediated rat liver transduction

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Cotugno, Gabriella ^a,b   Annunziata, Patrizia ^a,b   Barone, Maria Vittoria ^b   Karali, Marianthi ^a   Banfi, Sandro ^a,c   Auricchio, Alberto ^a,b  

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

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^c SECOND UNIVERSITY OF NAPLES   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ENHANCED GREEN FLUORESCENT PROTEIN; GLYCOSAMINOGLYCAN; MICRORNA; N ACETYLGALACTOSAMINE 4 SULFATASE; PARVOVIRUS VECTOR; THYROXINE BINDING GLOBULIN; GREEN FLUORESCENT PROTEIN; OLIGONUCLEOTIDE; RECOMBINANT DNA;

ADENO ASSOCIATED VIRUS; AGE; ANIMAL EXPERIMENT; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DILUTION; ENDOTHELIUM CELL; GENE EXPRESSION; GENE THERAPY; GENETIC TRANSDUCTION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; KIDNEY PARENCHYMA; KUPFFER CELL; LIVER CELL; LYSOSOME STORAGE DISEASE; NONHUMAN; NUCLEOTIDE SEQUENCE; RAT; REGULATORY SEQUENCE; SPLEEN; TRANSGENE; VIRAL GENE DELIVERY SYSTEM; WOODCHUCK HEPATITIS VIRUS; ANIMAL; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE VECTOR; GENETICS; LIVER DISEASE; LYSOSOME; METABOLISM; METHODOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ADENO-ASSOCIATED VIRUS; ANIMALIA; RATTUS; WOODCHUCK HEPATITIS VIRUS;

AGE FACTORS; ANIMALS; BLOTTING, WESTERN; DEPENDOVIRUS; DNA, RECOMBINANT; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE THERAPY; GENETIC VECTORS; GLYCOSAMINOGLYCANS; GREEN FLUORESCENT PROTEINS; LIVER DISEASES; LYSOSOMES; OLIGONUCLEOTIDES; RATS; REGULATORY ELEMENTS, TRANSCRIPTIONAL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSDUCTION, GENETIC; TRANSGENES;

EID: 84858124123     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0033286     Document Type: Article

References (75)

1. LoDuca PA, Hoffman BE, Herzog RW, (2009) Hepatic gene transfer as a means of tolerance induction to transgene products. Curr Gene Ther 9: 104-114.
2. Blouin A, Bolender RP, Weibel ER, (1977) Distribution of organelles and membranes between hepatocytes and nonhepatocytes in the rat liver parenchyma. A stereological study. J Cell Biol 72: 441-455.
3. Thomson AW, Knolle PA, (2010) Antigen-presenting cell function in the tolerogenic liver environment. Nat Rev Immunol 10: 753-766.
4. McKay TR, Rahim AA, Buckley SMK, Ward NJ, Chan JKY, et al. (2011) Perinatal Gene Transfer to the Liver. Current Pharmaceutical Design 17: 1-14.
5. Mingozzi F, High KA, (2011) Therapeutic in vivo gene transfer for genetic disease using AAV: progress and challenges. Nat Rev Genet 12: 341-355.
6. Nathwani AC, Rosales C, McIntosh J, Riddell A, Rustagi P, et al. (2010) Early clinical trial results following administration of a low dose of a novel self complementary adenoassociated viral vector encoding human factor ix in two subjects with severe Haemophilia B. XVIII Annual Congress of the European Society of Gene and Cell Therapy (ESGCT) Milan, Italy Mary Ann Liebert, Inc.
7. Ponder KP, (2011) Hemophilia gene therapy: a holy grail found. Mol Ther 19: 427-428.
8. McCarty DM, Young SM, Samulski RJ, (2004) Integration of adeno-associated virus (AAV) and recombinant AAV vectors. Annu Rev Genet 38: 819-845.
9. Nakai H, Yant SR, Storm TA, Fuess S, Meuse L, et al. (2001) Extrachromosomal recombinant adeno-associated virus vector genomes are primarily responsible for stable liver transduction in vivo. J Virol 75: 6969-6976.
10. Mehal WZ, Azzaroli F, Crispe IN, (2001) Immunology of the healthy liver: old questions and new insights. Gastroenterology 120: 250-260.
11. Wick MJ, Leithauser F, Reimann J, (2002) The hepatic immune system. Crit Rev Immunol 22: 47-103.
12. Ponder KP, Wang B, Wang P, Ma X, Herati R, et al. (2006) Mucopolysaccharidosis I cats mount a cytotoxic T lymphocyte response after neonatal gene therapy that can be blocked with CTLA4-Ig. Mol Ther 14: 5-13.
13. Xu L, Mei M, Haskins ME, Nichols TC, O'Donnell P, et al. (2007) Immune response after neonatal transfer of a human factor IX-expressing retroviral vector in dogs, cats, and mice. Thromb Res 120: 269-280.
14. Tessitore A, Faella A, O'Malley T, Cotugno G, Doria M, et al. (2008) Biochemical, pathological, and skeletal improvement of mucopolysaccharidosis VI after gene transfer to liver but not to muscle. Mol Ther 16: 30-37.
15. Cotugno G, Tessitore A, Capalbo A, Annunziata P, Strisciuglio C, et al. (2010) Different serum enzyme levels are required to rescue the various systemic features of the mucopolysaccharidoses. Hum Gene Ther 21: 555-569.
16. Ill CR, Yang CQ, Bidlingmaier SM, Gonzales JN, Burns DS, et al. (1997) Optimization of the human factor VIII complementary DNA expression plasmid for gene therapy of hemophilia A. Blood Coagul Fibrinolysis 8 (Suppl 2): S23-30.
17. Xiao W, Berta SC, Lu MM, Moscioni AD, Tazelaar J, et al. (1998) Adeno-associated virus as a vector for liver-directed gene therapy. J Virol 72: 10222-10226.
18. Wang L, Takabe K, Bidlingmaier SM, Ill CR, Verma IM, (1999) Sustained correction of bleeding disorder in hemophilia B mice by gene therapy. Proc Natl Acad Sci U S A 96: 3906-3910.
19. Franco LM, Sun B, Yang X, Bird A, Zhang H, et al. (2005) Evasion of immune responses to introduced human acid alpha-glucosidase by liver-restricted expression in glycogen storage disease type II. Mol Ther 12: 876-884.
20. Kitajima K, Marchadier DH, Burstein H, Rader DJ, (2006) Persistent liver expression of murine apoA-l using vectors based on adeno-associated viral vectors serotypes 5 and 1. Atherosclerosis 186: 65-73.
21. Moscioni D, Morizono H, McCarter RJ, Stern A, Cabrera-Luque J, et al. (2006) 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 14: 25-33.
22. Wang L, Calcedo R, Wang H, Bell P, Grant R, et al. (2010) The pleiotropic effects of natural AAV infections on liver-directed gene transfer in macaques. Mol Ther 18: 126-134.
23. Wang L, Wang H, Bell P, McCarter RJ, He J, et al. (2010) Systematic evaluation of AAV vectors for liver directed gene transfer in murine models. Mol Ther 18: 118-125.
24. Carrillo-Carrasco N, Chandler RJ, Chandrasekaran S, Venditti CP, (2010) 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 21: 1147-1154.
25. Bell P, Gao G, Haskins ME, Wang L, Sleeper MM, et al. (2011) Evaluation of AAV Vectors for Liver-directed Gene Transfer in Dogs. Hum Gene Ther.
26. Brown BD, Gentner B, Cantore A, Colleoni S, Amendola M, et al. (2007) Endogenous microRNA can be broadly exploited to regulate transgene expression according to tissue, lineage and differentiation state. Nat Biotechnol 25: 1457-1467.
27. Donello JE, Loeb JE, Hope TJ, (1998) Woodchuck hepatitis virus contains a tripartite posttranscriptional regulatory element. J Virol 72: 5085-5092.
28. Somanathan S, Breous E, Bell P, Wilson JM, (2010) AAV vectors avoid inflammatory signals necessary to render transduced hepatocyte targets for destructive T cells. Mol Ther 18: 977-982.
29. Carreras MC, Converso DP, Lorenti AS, Barbich M, Levisman DM, et al. (2004) Mitochondrial nitric oxide synthase drives redox signals for proliferation and quiescence in rat liver development. Hepatology 40: 157-166.
30. Cunningham SC, Dane AP, Spinoulas A, Logan GJ, Alexander IE, (2008) Gene delivery to the juvenile mouse liver using AAV2/8 vectors. Mol Ther 16: 1081-1088.
31. Flageul M, Aubert D, Pichard V, Nguyen TH, Nowrouzi A, et al. (2009) Transient expression of genes delivered to newborn rat liver using recombinant adeno-associated virus 2/8 vectors. J Gene Med 11: 689-696.
32. Dahms NM, Lobel P, Kornfeld S, (1989) Mannose 6-phosphate receptors and lysosomal enzyme targeting. J Biol Chem 264: 12115-12118.
33. Neufeld E, Muenzer J, (2001) The mucopolysaccharidoses. In: Scriver CRB, AL, Sly WS, Valle D, editors. New York McGraw-Hill pp. 4312-4352.
34. Cotugno G, Annunziata P, Tessitore A, O'Malley T, Capalbo A, et al. (2011) Long-term Amelioration of Feline Mucopolysaccharidosis VI After AAV-mediated Liver Gene Transfer. Mol Ther 19: 461-469.
35. Brown BD, Cantore A, Annoni A, Sergi LS, Lombardo A, et al. (2007) A microRNA-regulated lentiviral vector mediates stable correction of hemophilia B mice. Blood 110: 4144-4152.
36. Zufferey R, Donello JE, Trono D, Hope TJ, (1999) Woodchuck hepatitis virus posttranscriptional regulatory element enhances expression of transgenes delivered by retroviral vectors. J Virol 73: 2886-2892.
37. Loeb JE, Cordier WS, Harris ME, Weitzman MD, Hope TJ, (1999) Enhanced expression of transgenes from adeno-associated virus vectors with the woodchuck hepatitis virus posttranscriptional regulatory element: implications for gene therapy. Hum Gene Ther 10: 2295-2305.
38. Paterna JC, Moccetti T, Mura A, Feldon J, Bueler H, (2000) Influence of promoter and WHV post-transcriptional regulatory element on AAV-mediated transgene expression in the rat brain. Gene Ther 7: 1304-1311.
39. Glover CP, Bienemann AS, Heywood DJ, Cosgrave AS, Uney JB, (2002) Adenoviral-mediated, high-level, cell-specific transgene expression: a SYN1-WPRE cassette mediates increased transgene expression with no loss of neuron specificity. Mol Ther 5: 509-516.
40. Klein RL, Hamby ME, Sonntag CF, Millard WJ, King MA, et al. (2002) Measurements of vector-derived neurotrophic factor and green fluorescent protein levels in the brain. Methods 28: 286-292.
41. Appleby CE, Kingston PA, David A, Gerdes CA, Umana P, et al. (2003) A novel combination of promoter and enhancers increases transgene expression in vascular smooth muscle cells in vitro and coronary arteries in vivo after adenovirus-mediated gene transfer. Gene Ther 10: 1616-1622.
42. Xu ZL, Mizuguchi H, Mayumi T, Hayakawa T, (2003) Woodchuck hepatitis virus post-transcriptional regulation element enhances transgene expression from adenovirus vectors. Biochim Biophys Acta 1621: 266-271.
43. Glover CP, Bienemann AS, Hopton M, Harding TC, Kew JN, et al. (2003) Long-term transgene expression can be mediated in the brain by adenoviral vectors when powerful neuron-specific promoters are used. J Gene Med 5: 554-559.
44. Brun S, Faucon-Biguet N, Mallet J, (2003) Optimization of transgene expression at the posttranscriptional level in neural cells: implications for gene therapy. Mol Ther 7: 782-789.
45. Lipshutz GS, Titre D, Brindle M, Bisconte AR, Contag CH, et al. (2003) Comparison of gene expression after intraperitoneal delivery of AAV2 or AAV5 in utero. Mol Ther 8: 90-98.
46. Mian A, McCormack WM, Mane V, Kleppe S, Ng P, et al. (2004) Long-term correction of ornithine transcarbamylase deficiency by WPRE-mediated overexpression using a helper-dependent adenovirus. Mol Ther 10: 492-499.
47. Chtarto A, Yang X, Bockstael O, Melas C, Blum D, et al. (2007) Controlled delivery of glial cell line-derived neurotrophic factor by a single tetracycline-inducible AAV vector. Exp Neurol 204: 387-399.
48. Sims K, Ahmed Z, Gonzalez AM, Read ML, Cooper-Charles L, et al. (2008) Targeting adenoviral transgene expression to neurons. Mol Cell Neurosci 39: 411-417.
49. Puntel M, Barrett RJ, Mondkar S, Saxena V, Kroeger KM, et al. (2009) Herpes simplex virus type 1 thymidine kinase sequence fused to the lacz gene increases levels of {beta}-galactosidase activity per genome of high-capacity but not first-generation adenoviral vectors in vitro and in vivo. J Virol 83: 2004-2010.
50. Sun J, Li D, Hao Y, Zhang Y, Fan W, et al. (2009) Posttranscriptional regulatory elements enhance antigen expression and DNA vaccine efficacy. DNA Cell Biol 28: 233-240.
51. Zanta-Boussif MA, Charrier S, Brice-Ouzet A, Martin S, Opolon P, et al. (2009) Validation of a mutated PRE sequence allowing high and sustained transgene expression while abrogating WHV-X protein synthesis: application to the gene therapy of WAS. Gene Ther 16: 605-619.
52. Wei Y, Etiemble J, Fourel G, Vitvitski-Trepo L, Buendia MA, (1995) Hepadna virus integration generates virus-cell cotranscripts carrying 3′ truncated X genes in human and woodchuck liver tumors. J Med Virol 45: 82-90.
53. Kingsman SM, Mitrophanous K, Olsen JC, (2005) Potential oncogene activity of the woodchuck hepatitis post-transcriptional regulatory element (WPRE). Gene Ther 12: 3-4.
54. Schambach A, Bohne J, Baum C, Hermann FG, Egerer L, et al. (2006) Woodchuck hepatitis virus post-transcriptional regulatory element deleted from X protein and promoter sequences enhances retroviral vector titer and expression. Gene Ther 13: 641-645.
55. Mingozzi F, Liu YL, Dobrzynski E, Kaufhold A, Liu JH, et al. (2003) Induction of immune tolerance to coagulation factor IX antigen by in vivo hepatic gene transfer. J Clin Invest 111: 1347-1356.
56. Zhang HG, High KA, Wu Q, Yang P, Schlachterman A, et al. (2005) Genetic analysis of the antibody response to AAV2 and factor IX. Mol Ther 11: 866-874.
57. Sabatino DE, Mackenzie TC, Peranteau W, Edmonson S, Campagnoli C, et al. (2007) 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 15: 1677-1685.
58. Magami Y, Azuma T, Inokuchi H, Kokuno S, Moriyasu F, et al. (2002) Cell proliferation and renewal of normal hepatocytes and bile duct cells in adult mouse liver. Liver 22: 419-425.
59. Kiselyov K, Jennigs JJ, Rbaibi Y, Chu CT, (2007) Autophagy, mitochondria and cell death in lysosomal storage diseases. Autophagy 3: 259-262.
60. Settembre C, Fraldi A, Rubinsztein DC, Ballabio A, (2008) Lysosomal storage diseases as disorders of autophagy. Autophagy 4: 113-114.
61. Tessitore A, Pirozzi M, Auricchio A, (2009) Abnormal autophagy, ubiquitination, inflammation and apoptosis are dependent upon lysosomal storage and are useful biomarkers of mucopolysaccharidosis VI. Pathogenetics 2: 4.
62. Brown BD, Venneri MA, Zingale A, Sergi Sergi L, Naldini L, (2006) Endogenous microRNA regulation suppresses transgene expression in hematopoietic lineages and enables stable gene transfer. Nat Med 12: 585-591.
63. Haberman RP, McCown TJ, Samulski RJ, (2000) Novel transcriptional regulatory signals in the adeno-associated virus terminal repeat A/D junction element. J Virol 74: 8732-8739.
64. Jooss K, Yang Y, Fisher KJ, Wilson JM, (1998) Transduction of dendritic cells by DNA viral vectors directs the immune response to transgene products in muscle fibers. J Virol 72: 4212-4223.
65. Margolin KA, Negrin RS, Wong KK, Chatterjee S, Wright C, et al. (1997) Cellular immunotherapy and autologous transplantation for hematologic malignancy. Immunol Rev 157: 231-240.
66. Lu Y, Song S, (2009) Distinct immune responses to transgene products from rAAV1 and rAAV8 vectors. Proc Natl Acad Sci U S A 106: 17158-17162.
67. Ramezani A, Hawley TS, Hawley RG, (2000) Lentiviral vectors for enhanced gene expression in human hematopoietic cells. Mol Ther 2: 458-469.
68. Hlavaty J, Schittmayer M, Stracke A, Jandl G, Knapp E, et al. (2005) Effect of posttranscriptional regulatory elements on transgene expression and virus production in the context of retrovirus vectors. Virology 341: 1-11.
69. Klein R, Ruttkowski B, Knapp E, Salmons B, Gunzburg WH, et al. (2006) WPRE-mediated enhancement of gene expression is promoter and cell line specific. Gene 372: 153-161.
70. Schambach A, Wodrich H, Hildinger M, Bohne J, Krausslich HG, et al. (2000) Context dependence of different modules for posttranscriptional enhancement of gene expression from retroviral vectors. Mol Ther 2: 435-445.
71. Mautino MR, Morgan RA, (2002) Enhanced inhibition of human immunodeficiency virus type 1 replication by novel lentiviral vectors expressing human immunodeficiency virus type 1 envelope antisense RNA. Hum Gene Ther 13: 1027-1037.
72. Kraunus J, Schaumann DH, Meyer J, Modlich U, Fehse B, et al. (2004) Self-inactivating retroviral vectors with improved RNA processing. Gene Ther 11: 1568-1578.
73. Werner M, Kraunus J, Baum C, Brocker T, (2004) B-cell-specific transgene expression using a self-inactivating retroviral vector with human CD19 promoter and viral post-transcriptional regulatory element. Gene Ther 11: 992-1000.
74. Mangeot PE, Duperrier K, Negre D, Boson B, Rigal D, et al. (2002) High levels of transduction of human dendritic cells with optimized SIV vectors. Mol Ther 5: 283-290.
75. Breckpot K, Dullaers M, Bonehill A, van Meirvenne S, Heirman C, et al. (2003) Lentivirally transduced dendritic cells as a tool for cancer immunotherapy. J Gene Med 5: 654-667.