Partial correction of the CNS lysosomal storage defect in a mouse model of juvenile neuronal ceroid lipofuscinosis by neonatal CNS administration of an adeno-associated virus serotype rh.10 vector expressing the human CLN3 gene

Human Gene Therapy

Volumn 25, Issue 3, 2014, Pages 223-239

  Sondhi, Dolan ^a   Scott, Emma C ^a   Chen, Alvin ^a   Hackett, Neil R ^a   Wong, Andrew M S ^b   Kubiak, Agnieszka ^b   Nelvagal, Hemanth R ^b   Pearse, Yewande ^b   Cotman, Susan L ^c   Cooper, Jonathan D ^b   Crystal, Ronald G ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENO ASSOCIATED VIRUS VECTOR SEROTYPE 10 PROTEIN CLN3; COMPLEMENTARY DNA; PARVOVIRUS VECTOR; PROTEIN; PROTEIN CLN3; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOSOMAL RECESSIVE DISORDER; BRAIN CORTEX; CELL COUNT; CENTRAL NERVOUS SYSTEM DISEASE; CLN3 GENE; CONTROLLED STUDY; DRUG EFFECT; GENE; GENE EXPRESSION; GENE MUTATION; GENE THERAPY; GENE TRANSFER; GLIOSIS; HIPPOCAMPUS; HUMAN; IMMUNODETECTION; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; LYSOSOME STORAGE DISEASE; MOUSE; NERVE CELL DEGENERATION; NEURONAL CEROID LIPOFUSCINOSIS; NEWBORN; NONHUMAN; PERIODIC ACID SCHIFF STAIN; SEROTYPE; TRANSGENE; VIRAL GENE DELIVERY SYSTEM;

ANIMALS; ANIMALS, NEWBORN; BRAIN; DEPENDOVIRUS; DISEASE MODELS, ANIMAL; GENE EXPRESSION; GENETIC VECTORS; HUMANS; IMMUNOHISTOCHEMISTRY; INJECTIONS; INTERNEURONS; LYSOSOMES; MEMBRANE GLYCOPROTEINS; MICE; MICE, KNOCKOUT; MOLECULAR CHAPERONES; NEUROGLIA; NEURONAL CEROID-LIPOFUSCINOSES; NEURONS; RNA, MESSENGER; TRANSGENES;

EID: 84896361627     PISSN: 10430342     EISSN: 15577422     Source Type: Journal    
DOI: 10.1089/hum.2012.253     Document Type: Article

References (63)

1. Anzai, Y., Hayashi, M., Fueki, N., et al. (2006). Protracted juvenile neuronal ceroid lipofuscinosis-an autopsy report and immunohistochemical analysis. Brain Dev. 28, 462-465.
2. Autti, T., Raininko, R., Santavuori, P., et al. (1997). MRI of neuronal ceroid lipofuscinosis. II. Postmortem MRI and his-topathological study of the brain in 16 cases of neuronal ceroid lipofuscinosis of juvenile or late infantile type. Neu-roradiology 39, 371-377.
3. Bible, E., Gupta, P., Hofmann, S.L., et al. (2004). Regional and cellular neuropathology in the palmitoyl protein thioesterase-1 null mutant mouse model of infantile neuronal ceroid li-pofuscinosis. Neurobiol. Dis. 16, 346-359.
4. Bowers, W.J., Breakefield, X.O., and Sena-Esteves, M. (2011). Genetic therapy for the nervous system. Hum. Mol. Genet. 20, R28-R41.
5. Bronson, R.T., Donahue, L.R., Johnson, K.R., et al. (1998). Neuronal ceroid lipofuscinosis (nclf), a new disorder of the mouse linked to chromosome 9. Am. J. Med. Genet. 77, 289-297.
6. Cao, Y., Espinola, J.A., Fossale, E., et al. (2006). Autophagy is disrupted in a knock-in mouse model of juvenile neuronal ceroid lipofuscinosis. J. Biol. Chem. 281, 20483-20493.
7. Cearley, C.N., and Wolfe, J.H. (2006). Transduction characteristics of adeno-associated virus vectors expressing cap serotypes 7, 8, 9, and Rh10 in the mouse brain. Mol. Ther. 13, 528-537.
8. Chang, M., Cooper, J.D., Sleat, D.E., et al. (2008). In-traventricular enzyme replacement improves disease pheno-types in a mouse model of late infantile neuronal ceroid lipofuscinosis. Mol. Ther. 16, 649-656
9. ClinicalTrials.gov. (2011). AAVRh.10 administered to children with late infantile neuronal ceroid lipofuscinosis with uncommon genotypes or moderate/severe impairment. Available at http://clinicaltrials.gov/ct2/show/ NCT01414985 (accessed September 2013).
10. Cotman, S.L., Vrbanac, V., Lebel, L.A., et al. (2002). Cln3(Deltaex7/8) knock-in mice with the common JNCL mutation exhibit progressive neurologic disease that begins before birth. Hum. Mol. Genet. 11, 2709-2721.
11. Crystal, R.G., Sondhi, D., Hackett, N.R., et al. (2004). Clinical protocol. Administration of a replication-deficient adeno-associated virus gene transfer vector expressing the human CLN2 cDNA to the brain of children with late infantile neuronal ceroid lipofuscinosis. Hum. Gene Ther. 15, 1131-1154.
12. Cuervo, A.M. (2004). Autophagy: in sickness and in health. Trends Cell Biol. 14, 70-77.
13. Daly, T.M., Okuyama, T., Vogler, C., et al. (1999a). Neonatal intramuscular injection with recombinant adeno-associated virus results in prolonged beta-glucuronidase expression in situ and correction of liver pathology in mucopolysacchar-idosis type VII mice. Hum. Gene Ther. 10, 85-94.
14. Daly, T.M., Vogler, C., Levy, B., et al. (1999b). Neonatal gene transfer leads to widespread correction of pathology in a murine model of lysosomal storage disease. Proc. Natl. Acad. Sci. USA 96, 2296-2300.
15. Fossale, E., Wolf, P., Espinola, J.A., et al. (2004). Membrane trafficking and mitochondrial abnormalities precede subunit c deposition in a cerebellar cell model of juvenile neuronal ceroid lipofuscinosis. BMC Neurosci. 5, 57.
16. Getty, A.L., and Pearce, D.A. (2011). Interactions of the proteins of neuronal ceroid lipofuscinosis: clues to function. Cell Mol. Life Sci. 68, 453-474.
17. Gritti, A. (2011). Gene therapy for lysosomal storage disorders. Expert Opin. Biol. Ther. 11, 1153-1167.
18. Haltia, M. (2006). The neuronal ceroid-lipofuscinoses: from past to present. Biochim. Biophys. Acta 1762, 850-856.
19. Herrmann, P., Druckrey-Fiskaaen, C., Kouznetsova, E., et al. (2008). Developmental impairments of select neurotransmit-ter systems in brains of Cln3(Deltaex7/8) knock-in mice, an animal model of juvenile neuronal ceroid lipofuscinosis. J. Neurosci. Res. 86, 1857-1870.
20. Hofman, I., Kohlschutter, A., Santavuori, P., et al. (1999). CLN3 juvenile NCL. In The Neuronal Ceroid Lipofuscinoses (Batten Disease). H.H. Goebel, ed. (IOS Press, Birmingham, AL), pp. 55-76.
21. Janson, C., McPhee, S., Bilaniuk, L., et al. (2002). Clinical protocol. Gene therapy of Canavan disease: AAV-2 vector for neurosurgical delivery of aspartoacylase gene (ASPA) to the human brain. Hum. Gene Ther. 13, 1391-1412.
22. Jarvela, I., Lehtovirta, M., Tikkanen, R., et al. (1999). Defective intracellular transport of CLN3 is the molecular basis of Batten disease (JNCL). Hum. Mol. Genet. 8, 1091-1098.
23. Jolly, R.D., Martinus, R.D., and Palmer, D.N. (1992). Sheep and other animals with ceroid-lipofuscinoses: their relevance to Batten disease. Am. J. Med. Genet. 42, 609-614.
24. Kuronen, M., Lehesjoki, A.E., Jalanko, A., et al. (2012). Selective spatiotemporal patterns of glial activation and neuron loss in the sensory thalamocortical pathways of neuronal ceroid lipofuscinosis 8 mice. Neurobiol. Dis. 47, 444-457.
25. Leone, P., Shera, D., McPhee, S.W., et al. (2012). Long-term follow-up after gene therapy for canavan disease. Sci. Transl. Med. 4, 165ra163.
26. Lerner, T.J. (2001). Positional cloning of the JNCL gene, CLN3. Adv. Genet. 45, 107-121.
27. Lo, W.D., Qu, G., Sferra, T.J., et al. (1999). Adeno-associated virus-mediated gene transfer to the brain: duration and modulation of expression. Hum. Gene Ther. 10, 201-213.
28. Mao, Q., Foster, B.J., Xia, H., et al. (2003). Membrane topology of CLN3, the protein underlying Batten disease. FEBS Lett. 541, 40-46.
29. Mark, M., Teletin, M., Antal, C., et al. (2007). Histopathology in mouse metabolic investigations. Curr. Protoc. Mol. Biol. Chapter 29, Unit 29B.4.
30. McManus, J.F. (1948). Histological and histochemical uses of periodic acid. Stain Technol. 23, 99-108.
31. Michalewski, M.P., Kaczmarski, W., Golabek, A.A., et al. (1999). Posttranslational modification of CLN3 protein and its possible functional implication. Mol. Genet. Metab. 66, 272-276.
32. Mingozzi, F., and High, K.A. (2011). Therapeutic in vivo gene transfer for genetic disease using AAV: progress and challenges. Nat. Rev. Genet. 12, 341-355.
33. Mitchison, H.M., Bernard, D.J., Greene, N.D., et al. (1999). Targeted disruption of the Cln3 gene provides a mouse model for Batten disease. The Batten Mouse Model Consortium [corrected]. Neurobiol. Dis. 6, 321-334.
34. Munroe, P.B., Mitchison, H.M., O'Rawe, A.M., et al. (1997). Spectrum of mutations in the Batten disease gene, CLN3. Am. J. Hum. Genet. 61, 310-316.
35. Neufeld, E.F., and Fratantoni, J.C. (1970). Inborn errors of mucopolysaccharide metabolism. Science 169, 141-146.
36. Norton, W.T., Aquino, D.A., Hozumi, I., et al. (1992). Quantitative aspects of reactive gliosis: a review. Neurochem. Res. 17, 877-885.
37. Palmer, D.N., Fearnley, I.M., Walker, J.E., et al. (1992). Mitochondrial ATP synthase subunit c storage in the ceroid-lipofuscinoses (Batten disease). Am. J. Med. Genet. 42, 561-567.
38. Paxinos, G., and Franklin, K.B.J. (2001). The Mouse Brain in Stereotaxic Coordinates (Academic Press, San Diego, CA).
39. Petersen, A., Larsen, K.E., Behr, G.G., et al. (2001). Expanded CAG repeats in exon 1 of the Huntington's disease gene stimulate dopamine-mediated striatal neuron autophagy and degeneration. Hum. Mol. Genet. 10, 1243-1254.
40. Polito, V.A., Abbondante, S., Polishchuk, R.S., et al. (2010). Correction of CNS defects in the MPSII mouse model via systemic enzyme replacement therapy. Hum. Mol. Genet. 19, 4871-4885.
41. Pontikis, C.C., Cella, C.V., Parihar, N., et al. (2004). Late onset neurodegeneration in the Cln3-/-mouse model of juvenile neuronal ceroid lipofuscinosis is preceded by low level glial activation. Brain Res. 1023, 231-242.
42. Pontikis, C.C., Cotman, S.L., MacDonald, M.E., et al. (2005). Thalamocortical neuron loss and localized astrocytosis in the Cln3Deltaex7/8 knock-in mouse model of Batten disease. Neurobiol. Dis. 20, 823-836.
43. Puntel, M., Kroeger, K.M., Sanderson, N.S., et al. (2010). Gene transfer into rat brain using adenoviral vectors. Curr. Protoc. Neurosci. Chapter 4, Unit 4.24.
44. Rafi, M.A., Rao, H.Z., Luzi, P., et al. (2012). Extended normal life after AAVrh10-mediated gene therapy in the mouse model of Krabbe disease. Mol. Ther. 20, 2031-2042.
45. Rakheja, D., Narayan, S.B., and Bennett, M.J. (2008). The function of CLN3P, the Batten disease protein. Mol. Genet. Metab. 93, 269-274.
46. Sands, M.S., and Davidson, B.L. (2006). Gene therapy for ly-sosomal storage diseases. Mol. Ther. 13, 839-849.
47. Savas, P.S., Hemsley, K.M., and Hopwood, J.J. (2004). In-tracerebral injection of sulfamidase delays neuropathology in murine MPS-IIIA. Mol. Genet. Metab. 82, 273-285.
48. Sinha, S., Satishchandra, P., Santosh, V., et al. (2004). Neuronal ceroid lipofuscinosis: a clinicopathological study. Seizure 13, 235-240.
49. Sondhi, D., Peterson, D.A., Giannaris, E.L., et al. (2005). AAV2-mediated CLN2 gene transfer to rodent and non-human primate brain results in long-term TPP-I expression compatible with therapy for LINCL. Gene Ther. 12, 1618-1632.
50. Sondhi, D., Hackett, N.R., Peterson, D.A., et al. (2007). Enhanced survival of the LINCL mouse following CLN2 gene transfer using the rh.10 rhesus macaque-derived adeno-associated virus vector. Mol. Ther. 15, 481-491.
51. Sondhi, D., Peterson, D.A., Edelstein, A.M., et al. (2008). Survival advantage of neonatal CNS gene transfer for late infantile neuronal ceroid lipofuscinosis. Exp. Neurol. 213, 18-27.
52. Sondhi, D., Hackett, N.R., Scott, E., et al. (2011). Correction of the lysosomal storage defect in mouse model of juvenile neuronal ceroid lipofuscinosis by neonatal injection of AAV serotype rh.10 vector expressing the human CLN3 gene. Mol. Ther. 19[Supplement 1], S78.
53. Staropoli, J.F., Haliw, L., Biswas, S., et al. (2012). Large-scale phenotyping of an accurate genetic mouse model of JNCL identifies novel early pathology outside the central nervous system. PLoS One 7, e38310.
54. Stefanis, L., Larsen, K.E., Rideout, H.J., et al. (2001). Expression of A53T mutant but not wild-type alpha-synuclein in PC12 cells induces alterations of the ubiquitin-dependent degradation system, loss of dopamine release, and autophagic cell death. J. Neurosci. 21, 9549-9560.
55. The International Batten Disease Consortium. (1995). Isolation of a novel gene underlying Batten disease, CLN3. Cell 82, 949-957.
56. Tomanin, R., Zanetti, A., Zaccariotto, E., et al. (2012). Gene therapy approaches for lysosomal storage disorders, a good model for the treatment of mendelian diseases. Acta Paediatr. 101, 692-701.
57. Tyynela, J., Cooper, J.D., Khan, M.N., et al. (2004). Hippocampal pathology in the human neuronal ceroid-lipofuscinoses: distinct patterns of storage deposition, neurodegeneration and glial activation. Brain Pathol. 14, 349-357.
58. Waddington, S.N., Kennea, N.L., Buckley, S.M., et al. (2004). Fetal and neonatal gene therapy: benefits and pitfalls. Gene Ther. 11 Suppl. 1, S92-S97.
59. Weimer, J.M., Custer, A.W., Benedict, J.W., et al. (2006). Visual deficits in a mouse model of Batten disease are the result of optic nerve degeneration and loss of dorsal lateral geniculate thalamic neurons. Neurobiol. Dis. 22, 284-293.
60. Weimer, J.M., Yokota, Y., Stanco, A., et al. (2009). MARCKS modulates radial progenitor placement, proliferation and organization in the developing cerebral cortex. Development 136, 2965-2975.
61. West, M.J., Slomianka, L., and Gundersen, H.J. (1991). Unbiased stereological estimation of the total number of neurons in thesubdivisions of the rat hippocampus using the optical fractionator. Anat. Rec. 231, 482-497.
62. Worgall, S., Sondhi, D., Hackett, N.R., et al. (2008). Treatment of late infantile neuronal ceroid lipofuscinosis by CNS administration of a serotype 2 adeno-associated virus expressing CLN2 cDNA. Hum. Gene Ther. 19, 463-474.
63. Yu, W.H., Cuervo, A.M., Kumar, A., et al. (2005). Macro-autophagy-a novel Beta-amyloid peptide-generating pathway activated in Alzheimer's disease. J. Cell Biol. 171, 87-98.