Immunodominant liver-specific expression suppresses transgene-directed immune responses in murine pompe disease

Human Gene Therapy

Volumn 23, Issue 5, 2012, Pages 460-472

  Zhang, Ping ^a   Sun, Baodong ^a   Osada, Takuya ^a   Rodriguiz, Ramona ^a   Yang, Xiao Yi ^a   Luo, Xiaoyan ^a   Kemper, Alex R ^a   Clay, Timothy M ^a,b   Koeberl, Dwight D ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b GLAXOSMITHKLINE BIOLOGICALS   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CYTOKINE; GAMMA INTERFERON; GLUCAN 1,4 ALPHA GLUCOSIDASE; GLYCOGEN; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; IMMUNOGLOBULIN G1 ANTIBODY; IMMUNOLOGICAL ADJUVANT; INTERLEUKIN 12P40; INTERLEUKIN 1BETA; PARVOVIRUS VECTOR; TRANSCRIPTION FACTOR FOXP3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; CELL ACTIVATION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE RELEASE; DENDRITIC CELL; DRUG EFFICACY; ENHANCER REGION; ENZYME REPLACEMENT; GENE CASSETTE; GENE EXPRESSION; GENETIC TRANSDUCTION; GLYCOGEN STORAGE DISEASE TYPE 2; GRIP STRENGTH; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; LIVER; LYMPHOCYTE PROLIFERATION; MOTOR PERFORMANCE; MOUSE; MUSCLE FUNCTION; NONHUMAN; PROMOTER REGION; SPLEEN; T LYMPHOCYTE; TRANSGENE; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY;

ALPHA-GLUCOSIDASES; ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; DENDRITIC CELLS; DEPENDOVIRUS; ENZYME REPLACEMENT THERAPY; GENE THERAPY; GENETIC VECTORS; GLYCOGEN STORAGE DISEASE TYPE II; HUMANS; IMMUNE TOLERANCE; IMMUNOGLOBULIN G; INJECTIONS, INTRAVENOUS; LIVER; MICE; MICE, INBRED STRAINS; MICE, KNOCKOUT; ORGAN SPECIFICITY; T-LYMPHOCYTES; TRANSGENES;

MURINAE; MUS;

EID: 84861682930     PISSN: 10430342     EISSN: 15577422     Source Type: Journal    
DOI: 10.1089/hum.2011.063     Document Type: Article

References (38)

1. Allen, K.D., Griffin, T.M., Rodriguiz, R.M., et al. (2009). Decreased physical function and increased pain sensitivity in mice deficient for type IX collagen. Arthritis Rheum. 60, 2684-2693.
2. Amalfitano, A., McVie-Wylie, A.J., Hu, H., et al. (1999). Systemic correction of the muscle disorder glycogen storage disease type II after hepatic targeting of a modified adenovirus vector encoding human acid-a-glucosidase. Proc. Natl. Acad. Sci. U.S.A. 96, 8861-8866. (Pubitemid 29374673)
3. Amalfitano, A., Bengur, A.R., Morse, R.P., et al. (2001). Recombinant human acid a-glucosidase enzyme therapy for infantile glycogen storage disease type II: Results of a phase I/II clinical trial. Genet. Med. 3, 132-138.
4. Breous, E., Somanathan, S., Vandenberghe, L.H., and Wilson, J.M. (2009). Hepatic regulatory T cells and Kupffer cells are crucial mediators of systemic T cell tolerance to antigens targeting murine liver. Hepatology 50, 612-621.
5. Cao, O., Dobrzynski, E., Wang, L., et al. (2007). Induction and role of regulatory CD4+CD25+ T cells in tolerance to the transgene product following hepatic in vivo gene transfer. Blood 110, 1132-1140. (Pubitemid 47281408)
6. Ding, E., Hu, H., Hodges, B.L., et al. (2002). Efficacy of gene therapy for a prototypical lysosomal storage disease (GSD-II) is critically dependent on vector dose, transgene promoter, and the tissues targeted for vector transduction. Mol. Ther. 5, 436-446. (Pubitemid 34308669)
7. Ding, E.Y., Hodges, B.L., Hu, H., et al. (2001). Long-term efficacy after [E1-, polymerase-] adenovirus-mediated transfer of human acid-a-glucosidase gene into glycogen storage disease type II knockout mice. Hum. Gene Ther. 12, 955-965. (Pubitemid 32681859)
8. Duque, S., Joussemet, B., Riviere, C., et al. (2009). Intravenous administration of self-complementary AAV9 enables transgene delivery to adult motor neurons. Mol. Ther. 17, 1187-1196.
9. Franco, L.M., Sun, B., Yang, X., et al. (2005). Evasion of immune responses to introduced human acid a-glucosidase by liverrestricted expression in glycogen storage disease type II. Mol. Ther. 12, 876-884. (Pubitemid 41614483)
10. Gao, G.P., Alvira, M.R., Wang, L., et al. (2002). Novel adenoassociated viruses from rhesus monkeys as vectors for human gene therapy. Proc. Natl. Acad. Sci. U.S.A. 99, 11854-11859. (Pubitemid 34994488)
11. Hirschhorn, R., and Reuser, A.J.J. (2001) Glycogen storage disease type II: Acid a-glucosidase (acid maltase) deficiency. In C.R. Scriver, A.L. Beaudet, W.S. Sly, and D. Valle, eds. The Metabolic and Molecular Basis for Inherited Disease (McGraw-Hill, New York) pp. 3389-3419.
12. Hoffman, B.E., Dobrzynski, E., Wang, L., et al. (2007). Muscle as a target for supplementary factor IX gene transfer. Hum. Gene Ther. 18, 603-613. (Pubitemid 47187092)
13. Hunley, T.E., Corzo, D., Dudek, M., et al. (2004). Nephrotic syndrome complicating a-glucosidase replacement therapy for Pompe disease. Pediatrics 114, e532-e535. (Pubitemid 41529751)
14. Jooss, K., Yang, Y., Fisher, K.J., and Wilson, J.M. (1998). Transduction of dendritic cells by DNA viral vectors directs the immune response to transgene products in muscle fibers. J. Virol. 72, 4212-4223. (Pubitemid 28188726)
15. Kishnani, P.S., Hwu, W.L., Mandel, H., et al. (2006). A retrospective, multinational, multicenter study on the natural history of infantile-onset Pompe disease. J. Pediatr. 148, 671-676.
16. Kishnani, P.S., Goldenberg, P.C., Dearmey, S.L., et al. (2010). Crossreactive immunologic material status affects treatment outcomes in Pompe disease infants. Mol. Genet.Metab. 99, 26-33.
17. Koeberl, D.D., and Kishnani, P.S. (2009). Immunomodulatory gene therapy in lysosomal storage disorders. Curr. Gene Ther. 9, 503-510.
18. Loduca, P.A., Hoffman, B.E., and Herzog, R.W. (2009). Hepatic gene transfer as a means of tolerance induction to transgene products. Curr. Gene Ther. 9, 104-114.
19. Manno, C.S., Pierce, G.F., Arruda, V.R., et al. (2006). Successful transduction of liver in hemophilia by AAV-Factor IX and limitations imposed by the host immune response. Nat. Med. 12, 342-347. (Pubitemid 43355084)
20. Martiniuk, F., Mehler, M., Tzall, S., et al. (1990). Sequence of the cDNA and 5¢-flanking region for human acid a-glucosidase, detection of an intron in the 5¢ untranslated leader sequence, definition of 18-bp polymorphisms, and differences with previous cDNA and amino acid sequences. DNA Cell Biol. 9, 85-94. (Pubitemid 20125983)
21. Mays, L.E., and Wilson, J.M. (2011). The complex and evolving story of T cell activation to AAV vector-encoded transgene products. Mol. Ther. 19, 16-27.
22. Mendell, J.R., Campbell, K., Rodino-Klapac, L., et al. (2010). Dystrophin immunity in Duchenne's muscular dystrophy. N. Engl. J. Med. 363, 1429-1437.
23. Mingozzi, F., Liu, Y.L., Dobrzynski, E., et al. (2003). Induction of immune tolerance to coagulation factor IX antigen by in vivo hepatic gene transfer. J. Clin. Invest. 111, 1347-1356. (Pubitemid 36554705)
24. Ohshima, S., Shin, J.H., Yuasa, K., et al. (2009). Transduction efficiency and immune response associated with the administration of AAV8 vector into dog skeletal muscle. Mol. Ther. 17, 73-80.
25. Passini, M.A., Bu, J., Fidler, J.A., et al. (2007). Combination brain and systemic injections of AAV provide maximal functional and survival benefits in the Niemann-Pick mouse. Proc. Natl. Acad. Sci. U.S.A. 104, 9505-9510. (Pubitemid 47185809)
26. Ponce, E., Witte, D.P., Hirschhorn, R., et al. (1999). Murine acid aglucosidase: cell-specific mRNA differential expression during development and maturation. Am. J. Pathol. 154, 1089-1096. (Pubitemid 29169743)
27. Raben, N., Danon, M., Gilbert, A.L., et al. (2003). Enzyme replacement therapy in the mouse model of Pompe disease. Mol. Genet. Metab. 80, 159-169. (Pubitemid 37272242)
28. Ribar, T.J., Rodriguiz, R.M., Khiroug, L., et al. (2000). Cerebellar defects in Ca2 +calmodulin kinase IV-deficient mice. J. Neurosci. 20, RC107.
29. Sun, B., Zhang, H., Franco, L.M., et al. (2005a). Correction of glycogen storage disease type II by an adeno-associated virus vector containing a muscle-specific promoter. Mol. Ther. 11, 889-898. (Pubitemid 40724107)
30. Sun, B., Zhang, H., Franco, L.M., et al. (2005b). Efficacy of an adeno-associated virus 8-pseudotyped vector in glycogen storage disease type II. Mol. Ther. 11, 57-65. (Pubitemid 40011999)
31. Sun, B., Bird, A., Young, S.P., et al. (2007). Enhanced response to enzyme replacement therapy in Pompe disease after the induction of immune tolerance. Am. J. Hum. Genet. 81, 1042-1049. (Pubitemid 47580255)
32. Sun, B., Kulis, M.D., Young, S.P., et al. (2010). Immunomodulatory gene therapy prevents antibody formation and lethal hypersensitivity reactions in murine Pompe disease. Mol. Ther. 18, 353-360.
33. Wang, L., Takabe, K., Bidlingmaier, S.M., et al. (1999). Sustained correction of bleeding disorder in hemophilia B mice by gene therapy. Proc. Natl. Acad. Sci. U.S.A. 96, 3906-3910. (Pubitemid 29169009)
34. Wang, L., Nichols, T.C., Read, M.S., et al. (2000). Sustained expression of therapeutic level of factor IX in hemophilia B dogs by AAV-mediated gene therapy in liver. Mol. Ther. 1, 154-158.
35. Zaiss, A.K., Liu, Q., Bowen, G.P., et al. (2002). Differential activation of innate immune responses by adenovirus and adenoassociated virus vectors. J. Virol. 76, 4580-4590. (Pubitemid 34309593)
36. Zhang, Y., Chirmule, N., Gao, G., and Wilson, J. (2000). CD40 ligand-dependent activation of cytotoxic T lymphocytes by adeno-associated virus vectors in vivo: Role of immature dendritic cells. J. Virol. 74, 8003-8010. (Pubitemid 30641645)
37. Ziegler, R.J., Cherry, M., Barbon, C.M., et al. (2007). Correction of the biochemical and functional deficits in Fabry mice following AAV8-mediated hepatic expression of a-galactosidase A. Mol. Ther. 15, 492-500.
38. Ziegler, R.J., Bercury, S.D., Fidler, J., et al. (2008). Ability of adeno-associated virus serotype 8-mediated hepatic expression of acid a-glucosidase to correct the biochemical and motor function deficits of presymptomatic and symptomatic Pompe mice. Hum. Gene Ther. 19, 609-621. (Pubitemid 351913530)