Corrective GUSB transfer to the canine mucopolysaccharidosis VII cornea using a helper-dependent canine adenovirus vector

Journal of Controlled Release

Volumn 181, Issue 1, 2014, Pages 22-31

  Serratrice, Nicolas ^a,b   Cubizolle, Aurelie ^a,b   Ibanes, Sandy ^a,b   Mestre Francés, Nadine ^b,c,d   Bayo Puxan, Neus ^a,b   Creyssels, Sophie ^a,b   Gennetier, Aurelie ^a,b   Bernex, Florence ^e   Verdier, Jean Michel ^b,c,d   Haskins, Mark E ^f   Couderc, Guilhem ^g   Malecaze, Francois ^h,i   Kalatzis, Vasiliki ^a,b   Kremer, Eric J ^a,b  

^a INSTITUT DE GÉNÉTIQUE MOLÉCULAIRE DE MONTPELLIER   (France)

^b UNIV MONTPELLIER   (France)

^c University of Montpellier   (France)

^d PSL RESEARCH UNIVERSITY   (France)

^e CENTRE VAL D AURELLE   (France)

^f UNIVERSITY OF PENNSYLVANIA   (United States)

^g MONTPELLIER UNIVERSITY HOSPITAL   (France)

^h INSERM   (France)

ⁱ CHU PURPAN   (France)

Author keywords

Clouding; Cornea; Keratocytes; Lysosomal storage disorders; Mucopolysaccharidosis; Primates; Tissue engineering; Glucuronidase

Indexed keywords

CELL CULTURE; DIGITAL STORAGE; MAMMALS; TISSUE ENGINEERING;

CLOUDING; CORNEA; GLUCURONIDASE; KERATOCYTES; LYSOSOMAL STORAGE DISORDER; MUCOPOLYSACCHARIDOSIS; PRIMATES;

VECTORS;

ADENOVIRUS VECTOR; BETA GLUCURONIDASE; CANINE ADENOVIRUS TYPE 2 VECTOR; COMPLEMENTARY DNA; COXSACKIE VIRUS AND ADENOVIRUS RECEPTOR; UNCLASSIFIED DRUG; GLYCOSAMINOGLYCAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CANINE ADENOVIRUS; CONTROLLED STUDY; CORNEA; CORNEA CELL; COXSACKIE VIRUS; DNA TRANSFER; DOG; ENZYME ACTIVITY; EX VIVO STUDY; EXPLANT; FILM CASSETTE; GENETIC TRANSDUCTION; HISTOPATHOLOGY; HUMAN; HUMAN ADENOVIRUS 5; HUMAN TISSUE; IN VIVO STUDY; LYSOSOME; MOUSE; MUCOPOLYSACCHARIDOSIS TYPE 7; NONHUMAN; PATHOPHYSIOLOGY; PRIMATE; PRIORITY JOURNAL; VIRAL GENE DELIVERY SYSTEM; ANIMAL; C57BL MOUSE; CHEIROGALEIDAE; CONFOCAL MICROSCOPY; CORNEA STROMA; CORNEAL OPACITY; DISEASE MODEL; ENZYMOLOGY; GENE THERAPY; GENE TRANSFER; GENE VECTOR; GENETICS; HELPER VIRUS; HUMAN ADENOVIRUS; IN VITRO STUDY; METABOLISM; MUCOPOLYSACCHARIDOSIS VII; PATHOLOGY; SPECIES DIFFERENCE; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ADENOVIRUSES, CANINE; ADENOVIRUSES, HUMAN; ANIMALS; CHEIROGALEIDAE; CORNEAL OPACITY; CORNEAL STROMA; DISEASE MODELS, ANIMAL; DOGS; GENE TRANSFER TECHNIQUES; GENETIC THERAPY; GENETIC VECTORS; GLUCURONIDASE; GLYCOSAMINOGLYCANS; HELPER VIRUSES; HUMANS; IN VITRO TECHNIQUES; LYSOSOMES; MICE; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; MUCOPOLYSACCHARIDOSIS VII; SPECIES SPECIFICITY;

EID: 84896502187     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2014.02.022     Document Type: Article

References (50)

1. A. Mehta, and B. Winchester Lysosomal storage disorders 2013 Wiley-Blackwell West Susex
2. K.E. Bergwerk, R.E. Falk, B.J. Glasgow, and Y.S. Rabinowitz Corneal transplantation in a patient with mucopolysaccharidosis type VII (Sly disease) Ophthalmic Genet. 21 2000 17 20 (Pubitemid 30609503)
3. J. Muenzer Overview of the mucopolysaccharidoses Rheumatology 50 Suppl. 5 2011 v4 v12
4. E.F. Neufeld From serendipity to therapy Annu. Rev. Biochem. 80 2011 1 15
5. E.J. Kremer Gene transfer to the central nervous system: current state of the art of the viral vectors Curr. Genomics 6 2005 13 39
6. Y. Kamata, T. Okuyama, M. Kosuga, A. O'Hira, A. Kanaji, K. Sasaki, M. Yamada, and N. Azuma Adenovirus-mediated gene therapy for corneal clouding in mice with mucopolysaccharidosis type VII Mol. Ther. 4 2001 307 312 (Pubitemid 33040514)
7. T.S. Hnasko, F.A. Perez, A.D. Scouras, E.A. Stoll, S.D. Gale, S. Luquet, P.E. Phillips, E.J. Kremer, and R.D. Palmiter Cre recombinase-mediated restoration of nigrostriatal dopamine in dopamine-deficient mice reverses hypophagia and bradykinesia Proc. Natl. Acad. Sci. U. S. A. 103 2006 8858 8863 (Pubitemid 43878108)
8. C. Soudais, N. Skander, and E.J. Kremer Long-term in vivo transduction of neurons throughout the rat CNS using novel helper-dependent CAV-2 vectors FASEB J. 18 2004 391 393
9. M. Perreau, and E.J. Kremer Frequency, proliferation, and activation of human memory T cells induced by a nonhuman adenovirus J. Virol. 79 2005 14595 14605 (Pubitemid 41636258)
10. M. Perreau, M.C. Guerin, C. Drouet, and E.J. Kremer Interactions between human plasma components and a xenogenic adenovirus vector: reduced immunogenicity during gene transfer Mol. Ther. 15 2007 1998 2007 (Pubitemid 350011740)
11. M. Perreau, F. Mennechet, N. Serratrice, J.N. Glasgow, D.T. Curiel, H. Wodrich, and E.J. Kremer Contrasting effects of human, canine, and hybrid adenovirus vectors on the phenotypical and functional maturation of human dendritic cells: implications for clinical efficacy J. Virol. 81 2007 3272 3284 (Pubitemid 46456636)
12. E.H. Schuchman, T.K. Toroyan, M.E. Haskins, and R.J. Desnick Characterization of the defective beta-glucuronidase activity in canine mucopolysaccharidosis type VII Enzyme 42 1989 174 180 (Pubitemid 20069633)
13. E.J. Kremer, S. Boutin, M. Chillon, and O. Danos Canine adenovirus vectors: an alternative for adenovirus-mediated gene transfer J. Virol. 74 2000 505 512 (Pubitemid 30002932)
14. A. Cubizolle, N. Serratrice, N. Skander, M.A. Colle, S. Ibanes, A. Gennetier, N. Bayo-Puxan, K. Mazouni, F. Mennechet, B. Joussemet, Y. Cherel, Y. Lajat, C. Vite, F. Bernex, V. Kalatzis, M.E. Haskins, and E.J. Kremer Corrective GUSB transfer to the canine mucopolysaccharidosis VII brain Mol. Ther. 2013 10.1038/mt.2013.283
15. L. Ariza, L. Gimenez-Llort, A. Cubizolle, G. Pages, B. Garcia-Lareu, N. Serratrice, D. Cots, R. Thwaite, M. Chillon, E.J. Kremer, and A. Bosch Central nervous system delivery of helper-dependent canine adenovirus corrects neuropathology and behavior in mucopolysaccharidosis type VII mice Hum. Gene Ther. 2014 (in press)
16. C. Soudais, S. Boutin, and E.J. Kremer Characterization of cis-acting sequences involved in canine adenovirus packaging Mol. Ther. 3 2001 631 640 (Pubitemid 32509858)
17. W.S. Sly, B.A. Quinton, W.H. McAlister, and D.L. Rimoin Beta glucuronidase deficiency: report of clinical, radiologic, and biochemical features of a new mucopolysaccharidosis J. Pediatr. 82 1973 249 257
18. C. Hippert, S. Ibanes, N. Serratrice, F. Court, F. Malecaze, E.J. Kremer, and V. Kalatzis Corneal transduction by intra-stromal injection of AAV vectors in vivo in the mouse and ex vivo in human explants PLoS One 7 2012 e35318
19. M. Sosnova, M. Bradl, and J.V. Forrester CD34 + corneal stromal cells are bone marrow-derived and express hemopoietic stem cell markers Stem Cells 23 2005 507 515 (Pubitemid 40478490)
20. C. Soudais, S. Boutin, S.S. Hong, M. Chillon, O. Danos, J.M. Bergelson, P. Boulanger, and E.J. Kremer Canine adenovirus type 2 attachment and internalization: coxsackievirus-adenovirus receptor, alternative receptors, and an RGD-independent pathway J. Virol. 74 2000 10639 10649
21. J.M. Bergelson, J.A. Cunningham, G. Droguett, E.A. Kurt-Jones, A. Krithivas, J.S. Hong, M.S. Horwitz, R.L. Crowell, and R.W. Finberg Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5 Science 275 1997 1320 1323 (Pubitemid 27114163)
22. R. Tomko, R. Xu, and L. Philipson HCAR and MCAR: the human and mouse cellular receptors for subgroup C adenoviruses and group B cocksakieviruses Proc. Natl. Acad. Sci. 94 1997 3352 3356 (Pubitemid 27157315)
23. Y. Zhang, and J.M. Bergelson Adenovirus receptors J. Virol. 79 2005 12125 12131 (Pubitemid 41346076)
24. E.F. Neufeld Lysosomal storage diseases Annu. Rev. Biochem. 60 1991 257 280
25. M. Sardiello, M. Palmieri, A. di Ronza, D.L. Medina, M. Valenza, V.A. Gennarino, C. Di Malta, F. Donaudy, V. Embrione, R.S. Polishchuk, S. Banfi, G. Parenti, E. Cattaneo, and A. Ballabio A gene network regulating lysosomal biogenesis and function Science 325 2009 473 477
26. R.R. Mohan, J.C. Tovey, A. Sharma, and A. Tandon Gene therapy in the cornea: 2005-present Prog. Retin. Eye Res. 31 2012 43 64
27. T.Y. Lai, W.M. Chan, D.T. Liu, and D.S. Lam Ranibizumab for retinal angiomatous proliferation in neovascular age-related macular degeneration Graefes Arch. Clin. Exp. Ophthalmol. 245 2007 1877 1880 (Pubitemid 350154025)
28. H. Yu, J. Wu, H. Li, Z. Wang, X. Chen, Y. Tian, M. Yi, X. Ji, J. Ma, and Q. Huang Inhibition of corneal neovascularization by recombinant adenovirus-mediated sFlk-1 expression Biochem. Biophys. Res. Commun. 361 2007 946 952 (Pubitemid 47259027)
29. S. Saika, K. Ikeda, O. Yamanaka, T. Miyamoto, Y. Ohnishi, M. Sato, Y. Muragaki, A. Ooshima, Y. Nakajima, W.W. Kao, K.C. Flanders, and A.B. Roberts Expression of Smad7 in mouse eyes accelerates healing of corneal tissue after exposure to alkali Am. J. Pathol. 166 2005 1405 1418 (Pubitemid 40586511)
30. S.D. Galiacy, P. Fournie, D. Massoudi, E. Ancele, J.C. Quintyn, A. Erraud, I. Raymond-Letron, F. Rolling, and F. Malecaze Matrix metalloproteinase 14 overexpression reduces corneal scarring Gene Ther. 18 2011 462 468
31. K.A. Williams, and D.J. Coster Gene therapy for diseases of the cornea - a review Clin. Experiment. Ophthalmol. 38 2010 93 103
32. J. Alroy, M. Haskins, and D.E. Birk Altered corneal stromal matrix organization is associated with mucopolysaccharidosis I, III and VI Exp. Eye Res. 68 1999 523 530 (Pubitemid 29244138)
33. V. Kalatzis, N. Serratrice, C. Hippert, O. Payet, C. Arndt, C. Cazevieille, T. Maurice, C. Hamel, F. Malecaze, C. Antignac, A. Müller, and E.J. Kremer A temporospatial guide to the ocular anomalies in a cystinosis mouse model Pediatr. Res. 62 2 2007 Aug 156 162 (Pubitemid 47205713)
34. G. Nesterova, and W. Gahl Nephropathic cystinosis: late complications of a multisystemic disease Pediatr. Nephrol. 23 2008 863 878
35. S.U. Walkley Pathogenic cascades in lysosomal disease - why so complex? J. Inherit. Metab. Dis. 32 2009 181 189
36. R. Alba, A. Bosch, and M. Chillon Gutless adenovirus: last-generation adenovirus for gene therapy Gene Ther. 12 Suppl. 1 2005 S18 S27
37. A. Amalfitano, and R.J. Parks Separating fact from fiction: assessing the potential of modified adenovirus vectors for use in human gene therapy Curr. Gene Ther. 2 2002 111 133
38. R.R. Mohan, A.E. Hutcheon, R. Choi, J. Hong, J. Lee, R. Ambrosio Jr., J.D. Zieske, and S.E. Wilson Apoptosis, necrosis, proliferation, and myofibroblast generation in the stroma following LASIK and PRK Exp. Eye Res. 76 2003 71 87 (Pubitemid 36268717)
39. A.P. Bemelmans, Y. Arsenijevic, and F. Majo Efficient lentiviral gene transfer into corneal stroma cells using a femtosecond laser Gene Ther. 16 2009 933 938
40. M.E. Fini, and B.M. Stramer How the cornea heals: cornea-specific repair mechanisms affecting surgical outcomes Cornea 24 2005 S2 S11
41. C.W. Sindt, B. Lay, H. Bouchard, and J.R. Kern Rapid image evaluation system for corneal in vivo confocal microscopy Cornea 32 2013 460 465
42. E.C. Carlson, C.Y. Liu, X. Yang, M. Gregory, B. Ksander, J. Drazba, and V.L. Perez In vivo gene delivery and visualization of corneal stromal cells using an adenoviral vector and keratocyte-specific promoter Invest. Ophthalmol. Vis. Sci. 45 2004 2194 2200 (Pubitemid 38902589)
43. Y. Du, M.L. Funderburgh, M.M. Mann, N. SundarRaj, and J.L. Funderburgh Multipotent stem cells in human corneal stroma Stem Cells 23 2005 1266 1275 (Pubitemid 41504914)
44. C. Vogler, N. Galvin, B. Levy, J. Grubb, J. Jiang, X.Y. Zhou, and W.S. Sly Transgene produces massive overexpression of human beta-glucuronidase in mice, lysosomal storage of enzyme, and strain-dependent tumors Proc. Natl. Acad. Sci. U. S. A. 100 2003 2669 2673 (Pubitemid 36297556)
45. K.O. Orii, J.H. Grubb, C. Vogler, B. Levy, Y. Tan, K. Markova, B.L. Davidson, Q. Mao, T. Orii, N. Kondo, and W.S. Sly Defining the pathway for Tat-mediated delivery of beta-glucuronidase in cultured cells and MPS VII mice Mol. Ther. 12 2005 345 352 (Pubitemid 41025106)
46. S. Tomatsu, K.O. Orii, C. Vogler, J.H. Grubb, E.M. Snella, M. Gutierrez, T. Dieter, C.C. Holden, K. Sukegawa, T. Orii, N. Kondo, and W.S. Sly Production of MPS VII mouse (Gus(tm(hE540A.mE536A)Sly)) doubly tolerant to human and mouse beta-glucuronidase Hum. Mol. Genet. 12 2003 961 973 (Pubitemid 36553516)
47. J.H. Wolfe, M.S. Sands, N. Harel, M.A. Weil, M.K. Parente, A.C. Polesky, J.J. Reilly, C. Hasson, S. Weimelt, and M.E. Haskins Gene transfer of low levels of beta-glucuronidase corrects hepatic lysosomal storage in a large animal model of mucopolysaccharidosis VII Mol. Ther. 2 2000 552 561
48. J.L. Ashworth, S. Biswas, E. Wraith, and I.C. Lloyd Mucopolysaccharidoses and the eye Surv. Ophthalmol. 51 2006 1 17 (Pubitemid 43083370)
49. J.L. Ashworth, S. Biswas, E. Wraith, and I.C. Lloyd The ocular features of the mucopolysaccharidoses Eye 20 2006 553 563 (Pubitemid 43674991)
50. J. Seok, H.S. Warren, A.G. Cuenca, M.N. Mindrinos, H.V. Baker, W. Xu, D.R. Richards, G.P. McDonald-Smith, H. Gao, L. Hennessy, C.C. Finnerty, C.M. Lopez, S. Honari, E.E. Moore, J.P. Minei, J. Cuschieri, P.E. Bankey, J.L. Johnson, J. Sperry, A.B. Nathens, T.R. Billiar, M.A. West, M.G. Jeschke, M.B. Klein, R.L. Gamelli, N.S. Gibran, B.H. Brownstein, C. Miller-Graziano, S.E. Calvano, P.H. Mason, J.P. Cobb, L.G. Rahme, S.F. Lowry, R.V. Maier, L.L. Moldawer, D.N. Herndon, R.W. Davis, W. Xiao, and R.G. Tompkins Genomic responses in mouse models poorly mimic human inflammatory diseases Proc. Natl. Acad. Sci. U. S. A. 110 2013 3507 3512