Proteasome inhibition is partially effective in attenuating pre-existing immunity against recombinant adeno-associated viral vectors

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Karman, Jozsef ^a   Gumlaw, Nathan K ^a   Zhang, Jinhua ^a   Jiang, Ji Lei ^a   Cheng, Seng H ^a   Zhu, Yunxiang ^a  

^a GENZYME CORPORATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA GALACTOSIDASE; BORTEZOMIB; IMMUNOGLOBULIN G; PARVOVIRUS VECTOR; RECOMBINANT PARVOVIRUS 2 VECTOR; RECOMBINANT PARVOVIRUS 8 VECTOR; UNCLASSIFIED DRUG; BORONIC ACID DERIVATIVE; CYTOKINE; PROTEASOME; PYRAZINE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY TITER; ARTICLE; B LYMPHOCYTE ACTIVATION; BONE MARROW; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DRUG DOSE COMPARISON; DRUG EFFICACY; DRUG MECHANISM; ENZYME INHIBITION; GENETIC TRANSDUCTION; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOGLOBULIN PRODUCTION; IMMUNOSUPPRESSIVE TREATMENT; LYMPHOCYTE DEPLETION; LYMPHOID ORGAN; MALE; MEMORY CELL; MOUSE; NONHUMAN; PLASMA CELL; REINFECTION; SEROTYPE; VIRAL GENE DELIVERY SYSTEM; ADENO ASSOCIATED VIRUS; ANIMAL; DRUG ANTAGONISM; DRUG EFFECT; FLOW CYTOMETRY; GENE VECTOR; IMMUNITY; IMMUNOLOGY; METABOLISM;

ADENO-ASSOCIATED VIRUS; MUS;

ANIMALS; BORONIC ACIDS; CYTOKINES; DEPENDOVIRUS; FLOW CYTOMETRY; GENETIC VECTORS; IMMUNITY; MALE; MICE; PROTEASOME ENDOPEPTIDASE COMPLEX; PYRAZINES;

EID: 84859728188     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0034684     Document Type: Article

References (39)

1. Bainbridge JW, Smith AJ, Barker SS, Robbie S, Henderson R, et al. (2008) Effect of gene therapy on visual function in Leber's congenital amaurosis. N Engl J Med 358: 2231-2239.
2. Brantly ML, Spencer LT, Humphries M, Conlon TJ, Spencer CT, et al. (2006) Phase I trial of intramuscular injection of a recombinant adeno-associated virus serotype 2 alphal-antitrypsin (AAT) vector in AAT-deficient adults. Hum Gene Ther 17: 1177-1186.
3. Kaplitt MG, Feigin A, Tang C, Fitzsimons HL, Mattis P, et al. (2007) Safety and tolerability of gene therapy with an adeno-associated virus (AAV) borne GAD gene for Parkinson's disease: an open label, phase I trial. Lancet 369: 2097-2105.
4. Kay MA, Manno CS, Ragni MV, Larson PJ, Couto LB, et al. (2000) Evidence for gene transfer and expression of factor IX in haemophilia B patients treated with an AAV vector. Nat Genet 24: 257-261.
5. Maclachlan TK, Lukason M, Collins M, Munger R, Isenberger E, et al. (2011) Preclinical safety evaluation of AAV2-sFLT01- a gene therapy for age-related macular degeneration. Mol Ther 19: 326-334.
6. Chirmule N, Propert K, Magosin S, Qian Y, Qian R, et al. (1999) Immune responses to adenovirus and adeno-associated virus in humans. Gene Ther 6: 1574-1583.
7. McIntosh JH, Cochrane M, Cobbold S, Waldmann H, Nathwani SA, et al. (2012) Successful attenuation of humoral immunity to viral capsid and transgenic protein following AAV-mediated gene transfer with a non-depleting CD4 antibody and cyclosporine. Gene Ther 19: 78-85.
8. Montenegro-Miranda PS, ten Bloemendaal L, Kunne C, de Waart DR, Bosma PJ, (2011) Mycophenolate mofetil impairs transduction of single-stranded adeno-associated viral vectors. Hum Gene Ther 22: 605-612.
9. Curran MP, McKeage K, (2009) Bortezomib: a review of its use in patients with multiple myeloma. Drugs 69: 859-888.
10. Finn JD, Hui D, Downey HD, Dunn D, Pien GC, et al. (2010) Proteasome inhibitors decrease AAV2 capsid derived peptide epitope presentation on MHC class I following transduction. Mol Ther 18: 135-142.
11. Monahan PE, Lothrop CD, Sun J, Hirsch ML, Kafri T, et al. (2010) Proteasome inhibitors enhance gene delivery by AAV virus vectors expressing large genomes in hemophilia mouse and dog models: a strategy for broad clinical application. Mol Ther 18: 1907-1916.
12. Nathwani AC, Cochrane M, McIntosh J, Ng CY, Zhou J, et al. (2009) Enhancing transduction of the liver by adeno-associated viral vectors. Gene Ther 16: 60-69.
13. Neubert K, Meister S, Moser K, Weisel F, Maseda D, et al. (2008) The proteasome inhibitor bortezomib depletes plasma cells and protects mice with lupus-like disease from nephritis. Nat Med 14: 748-755.
14. Gu H, Chen X, Gao G, Dong H, (2008) Caspase-2 functions upstream of mitochondria in endoplasmic reticulum stress-induced apoptosis by bortezomib in human myeloma cells. Mol Cancer Ther 7: 2298-2307.
15. Meister S, Schubert U, Neubert K, Herrmann K, Burger R, et al. (2007) Extensive immunoglobulin production sensitizes myeloma cells for proteasome inhibition. Cancer Res 67: 1783-1792.
16. Ziegler RJ, Cherry M, Barbon CM, Li C, Bercury SD, et al. (2007) Correction of the biochemical and functional deficits in fabry mice following AAV8-mediated hepatic expression of alpha-galactosidase A. Mol Ther 15: 492-500.
17. Ziegler RJ, Lonning SM, Armentano D, Li C, Souza DW, et al. (2004) AAV2 vector harboring a liver-restricted promoter facilitates sustained expression of therapeutic levels of alpha-galactosidase A and the induction of immune tolerance in Fabry mice. Mol Ther 9: 231-240.
18. McEachern KA, Nietupski JB, Chuang WL, Armentano D, Johnson J, et al. (2006) AAV8-mediated expression of glucocerebrosidase ameliorates the storage pathology in the visceral organs of a mouse model of Gaucher disease. J Gene Med 8: 719-729.
19. Manis JP, Tian M, Alt FW, (2002) Mechanism and control of class-switch recombination. Trends Immunol 23: 31-39.
20. Amanna IJ, Slifka MK, (2010) Mechanisms that determine plasma cell lifespan and the duration of humoral immunity. Immunol Rev 236: 125-138.
21. Kloetzel PM, (2004) The proteasome and MHC class I antigen processing. Biochim Biophys Acta 1695: 225-233.
22. Kloetzel PM, Ossendorp F, (2004) Proteasome and peptidase function in MHC-class-I-mediated antigen presentation. Curr Opin Immunol 16: 76-81.
23. Chao H, Sun L, Bruce A, Xiao X, Walsh CE, (2002) Expression of human factor VIII by splicing between dimerized AAV vectors. Mol Ther 5: 716-722.
24. Grieger JC, Samulski RJ, (2005) Adeno-associated virus as a gene therapy vector: vector development, production and clinical applications. Adv Biochem Eng Biotechnol 99: 119-145.
25. Manno CS, Chew AJ, Hutchison S, Larson PJ, Herzog RW, et al. (2003) AAV-mediated factor IX gene transfer to skeletal muscle in patients with severe hemophilia B. Blood 101: 2963-2972.
26. Marshall J, McEachern KA, Kyros JA, Nietupski JB, Budzinski T, et al. (2002) Demonstration of feasibility of in vivo gene therapy for Gaucher disease using a chemically induced mouse model. Mol Ther 6: 179-189.
27. Nathwani AC, Rosales C, McIntosh J, Rastegarlari G, Nathwani D, et al. (2011) 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 Ther19: 876-885.
28. Xie Y, (2010) Structure, assembly and homeostatic regulation of the 26 S proteasome. J Mol Cell Biol 2: 308-317.
29. Obeng EA, Carlson LM, Gutman DM, Harrington WJ Jr, Lee KP, et al. (2006) Proteasome inhibitors induce a terminal unfolded protein response in multiple myeloma cells. Blood 107: 4907-4916.
30. Calame KL, (2001) Plasma cells: finding new light at the end of B cell development. Nat Immunol 2: 1103-1108.
31. McHeyzer-Williams LJ, McHeyzer-Williams MG, (2005) Antigen-specific memory B cell development. Annu Rev Immunol 23: 487-513.
32. Rajkumar SV, (2011) Multiple myeloma: 2011 update on diagnosis, risk-stratification, and management. Am J Hematol 86: 57-65.
33. Scallan CD, Jiang H, Liu T, Patarroyo-White S, Sommer JM, et al. (2006) Human immunoglobulin inhibits liver transduction by AAV vectors at low AAV2 neutralizing titers in SCID mice. Blood 107: 1810-1817.
34. Reagan-Shaw S, Nihal M, Ahmad N, (2008) Dose translation from animal to human studies revisited. FASEB J 22: 659-661.
35. Murphy SL, Li H, Zhou S, Schlachterman A, High KA, (2008) Prolonged susceptibility to antibody-mediated neutralization for adeno-associated vectors targeted to the liver. Mol Ther 16: 138-145.
36. Manning WC, Zhou S, Bland MP, Escobedo JA, Dwarki V, (1998) Transient immunosuppression allows transgene expression following readministration of adeno-associated viral vectors. Hum Gene Ther 9: 477-485.
37. Nathwani AC, Tuddenham EG, Rangarajan S, Rosales C, McIntosh J, et al. (2011) Adenovirus-associated virus vector-mediated gene transfer in hemophilia B. N Engl J Med 365: 2357-2365.
38. Attar EC, de Angelo DJ, Supko JG, D'Amato F, Zahrieh D, et al. (2008) Phase I and pharmacokinetic study of bortezomib in combination with idarubicin and cytarabine in patients with acute myelogenous leukemia. Clin Cancer Res 14: 1446-1454.
39. Hemeryck A, Geerts R, Monbaliu J, Hassler S, Verhaeghe T, et al. (2007) Tissue distribution and depletion kinetics of bortezomib and bortezomib-related radioactivity in male rats after single and repeated intravenous injection of 14 C-bortezomib. Cancer Chemother Pharmacol 60: 777-787.