Treatment of late infantile neuronal ceroid lipofuscinosis by CNS administration of a serotype 2 adeno-associated virus expressing CLN2 cDNA

Human Gene Therapy

Volumn 19, Issue 5, 2008, Pages 463-474

  Worgall, Stefan ^a   Sondhi, Dolan ^a   Hackett, Neil R ^a   Kosofsky, Barry ^a   Kekatpure, Minal V ^a   Neyzi, Nurunisa ^a   Dyke, Jonathan P ^a   Ballon, Douglas ^a   Heier, Linda ^a   Greenwald, Bruce M ^a   Christos, Paul ^a   Mazumdar, Madhu ^a   Souweidane, Mark M ^a   Kaplitt, Michael G ^a   Crystal, Ronald G ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLN2 CDNA; PARVOVIRUS VECTOR; SERINE PROTEINASE;

ADENO ASSOCIATED VIRUS; ANEMIA; ARTICLE; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; DRUG EFFICACY; DRUG SAFETY; EPILEPTIC STATE; ERYTHROCYTE SEDIMENTATION RATE; FEMALE; HUMAN; HUMORAL IMMUNITY; MALE; MYOCLONUS; NEURONAL CEROID LIPOFUSCINOSIS; NUCLEAR MAGNETIC RESONANCE IMAGING; RATING SCALE; SEIZURE; SIDE EFFECT; THROMBOCYTOSIS; TREATMENT DURATION; TREATMENT OUTCOME; UNSPECIFIED SIDE EFFECT; VIRUS PARTICLE; VIRUS STRAIN; VOMITING;

ANTIBODIES, VIRAL; CENTRAL NERVOUS SYSTEM; CHILD; CHILD, PRESCHOOL; DEPENDOVIRUS; DISEASE PROGRESSION; DNA, COMPLEMENTARY; ENDOPEPTIDASES; FEMALE; FOLLOW-UP STUDIES; GENE THERAPY; GENETIC VECTORS; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; NEURONAL CEROID-LIPOFUSCINOSES;

ADENO-ASSOCIATED VIRUS;

EID: 44349136847     PISSN: 10430342     EISSN: None     Source Type: Journal    
DOI: 10.1089/hum.2008.022     Document Type: Article

References (38)

1. ARKIN, L.M., SONDHI, D., WORGALL, S., SUH, L.H., HACKETT, N.R., KAMINSKY, S.M., HOSAIN, S.A., SOUWEIDANE, M.M., KAPLITT, M.G., DYKE, J.P., HEIER, L.A., BALLON, D.J., SHUNGU, D.C., WISNIEWSKI, K.E., GREENWALD, B.M., HOLLMANN, C., and CRYSTAL, R.G. (2005). Confronting the issues of therapeutic misconception, enrollment decisions, and personal motives in genetic medicine-based clinical research studies for fatal disorders. Hum. Gene Ther. 16, 1028-1036.
2. BOHNEN, N.I., KUWABARA, H., CONSTANTINE, G.M., MATHIS, C.A., and MOORE, R.Y. (2007). Grooved pegboard test as a biomarker of nigrostriatal denervation in Parkinson's disease. Neurosci. Lett. 424, 185-189.
3. BOSCH, A., PERRET, E., DESMARIS, N., and HEARD, J.M. (2000). Long-term and significant correction of brain lesions in adult mucopolysaccharidosis type VII mice using recombinant AAV vectors. Mol. Ther. 1, 63-70.
4. BOUSTANY, R.M. (1996). Batten disease or neuronal ceroid lipofuscinosis. In Handbook of Clinical Neurology (Vol. 66 [22]): Neurodystrophies and Neurolipidoses, H.W. Moser, ed. (New York: Elsevier Science), pp. 671-700.
5. BROEKMAN, M.L., COMER, L.A., HYMAN, B.T., and SENA-ESTEVES, M. (2006). Adeno-associated virus vectors serotyped with AAV8 capsid are more efficient than AAV-1 or -2 serotypes for widespread gene delivery to the neonatal mouse brain. Neuroscience 138, 501-510.
6. BROUGH, D.E., LIZONOVA, A., HSU, C., KULESA, V.A., and KOVESDI, I. (1996). A gene transfer vector-cell line system for complete functional complementation of adenovirus early regions E1 and E4. J. Virol. 70, 6497-6501.
7. BUNNELL, B.A., DUFOUR, J., BELENCHIA, G., ALVAREZ, X., BAKER, K., DIDIER, P., LACKNER, A., and WOLFE, J. H. (2004). Assessment of the transduction patterns of alternative AAV vector serotypes in the CNS of rhesus macaques. Mol. Ther. 9, S129.
8. CABRERA-SALAZAR, M.A., ROSKELLEY, E.M., BU, J., HODGES, B.L., YEW, N., DODGE, J.C., SHIHABUDDIN, L.S., SOHAR, I., SLEAT, D.E., SCHEULE, R.K., DAVIDSON, B.L., CHENG, S.H., LOBEL, P., and PASSINI, M.A. (2007). Timing of therapeutic intervention determines functional and survival outcomes in a mouse model of late infantile batten disease. Mol. Ther. 15, 1782-1788.
9. 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.
10. CRESSANT, A., DESMARIS, N., VEROT, L., BREJOT, T., FROISSART, R., VANIER, M.T., MAIRE, I., and HEARD, J.M. (2004). Improved behavior and neuropathology in the mouse model of Sanfilippo type IIIB disease after adeno-associated virus-mediated gene transfer in the striatum. J. Neurosci. 24, 10229-10239.
11. CRYSTAL, R.G., SONDHI, D., HACKETT, N.R., KAMINSKY, S.M., WORGALL, S., STIEG, P., SOUWEIDANE, M., HOSAIN, S., HEIER, L., BALLON, D., DINNER, M., WISNIEWSKI, K., KAPLITT, M., GREENWALD, B.M., HOWELL, J.D., STRYBING, K., DYKE, J., and VOSS, H. (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. DYKE, J.P., VOSS, H.U., SONDHI, D., HACKETT, N.R., WORGALL, S., HEIER, L.A., KOSOFSKY, B.E., ULUG, A.M., SHUNGU, D.C., MAO, X., CRYSTAL, R.G., and BALLON, D. (2007). Assessing disease severity in late infantile neuronal ceroid lipofuscinosis using quantitative MR diffusion-weighted imaging. Am. J. Neuroradiol. 28, 1232-1236.
13. FRISELLA, W.A., O'CONNOR, L.H., VOGLER, C.A., ROBERTS, M., WALKLEY, S., LEVY, B., DALY, T.M., and SANDS, M.S. (2001). Intracranial injection of recombinant adeno-associated virus improves cognitive function in a murine model of mucopolysaccharidosis type VII. Mol. Ther. 3, 351-358.
14. GRIFFEY, M.A., WOZNIAK, D., WONG, M., BIBLE, E., JOHNSON, K., ROTHMAN, S.M., WENTZ, A.E., COOPER, J.D., and SANDS, M.S. (2006). CNS-directed AAV2-mediated gene therapy ameliorates functional deficits in a murine model of infantile neuronal ceroid lipofuscinosis. Mol. Ther. 13, 538-547.
15. HACKETT, N.R., REDMOND, D.E., SONDHI, D., GIANNARIS, E.L., VASSALLO, E., STRATTON, J., QIU, J., KAMINSKY, S.M., LESSER, M.L., FISCH, G.S., ROUSELLE, S.D., and CRYSTAL, R.G. (2005). Safety of direct administration of AAV2CUhCLN2, a candidate treatment for the central nervous system manifestations of late infantile neuronal ceroid lipofuscinosis, to the brain of rats and nonhuman primates. Hum. Gene Ther. 16, 1484-1503.
16. HALTIA, M. (2003). The neuronal ceroid-lipofuscinoses. J. Neuropathol. Exp. Neurol. 62, 1-13.
17. HASKELL, R.E., HUGHES, S.M., CHIORINI, J.A., ALISKY, J.M., and DAVIDSONS, B.L. (2003). Viral-mediated delivery of late-infantile neuronal ceroid lipofuscinosis gene, TPP-I to the mouse central nervous system. Gene Ther. 10, 34-42.
18. JANSON, C., McPHEE, S., BILANIUK, L., HASELGROVE, J., TESTAIUTI, M., FREESE, A., WANG, D.J., SHERA, D., HURH, P., RUPIN, J., SASLOW, E., GOLDFARB, O., GOLDBERG, M., LARIJANI, G., SHARRAR, W., LIOUTERMAN, L., CAMP, A., KOLODNY, E., SAMULSKI, J., and LEONE, P. (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.
19. KORZENIEWSKI, S.J., BIRBECK, G., DELANO, M.C., POTCHEN, M.J., and PANETH, N. (2008). A systematic review of neuroimaging for cerebral palsy. J. Child Neurol. 23, 216-227.
20. LANE, S.C., JOLLY, R.D., SCHMECHEL, D.E., ALROY, J., and BOUSTANY, R.M. (1996). Apoptosis as the mechanism of neurodegeneration in Batten's disease. J. Neurochem. 67, 677-683.
21. PASSINI, M.A., MACAULEY, S.L., HUFF, M.R., TAKSIR, T.V., BU, J., WU, I.H., PIEPENHAGEN, P.A., DODGE, J.C., SHIHABUDDIN, L.S., O'RIORDAN, C.R., SCHUCHMAN, E.H., and STEWART, G.R. (2005). AAV vector-mediated correction of brain pathology in a mouse model of Niemann-Pick A disease. Mol. Ther. 11, 754-762.
22. PASSINI, M.A., DODGE, J.C., BU, J., YANG, W., ZHAO, Q., SONDHI, D., HACKETT, N.R., KAMINSKY, S.M., MAO, Q., SHIHABUDDIN, L.S., CHENG, S.H., SLEAT, D.E., STEWART, G.R., DAVIDSON, B.L., LOBEL, P., and CRYSTAL, R.G. (2006). Intracranial delivery of CLN2 reduces brain pathology in a mouse model of classical late infantile neuronal ceroid lipofuscinosis. J. Neurosci. 26, 1334-1342.
23. QIU, J.P., MENDEZ, B.S., CRYSTAL, R.G., and HACKETT, N.R. (2002). Construction and verification of an Ad/AAV helper plasmid designed for manufacturing recombinant AAV vectors for administration. Mol. Ther. 5, S47.
24. RAMIREZ-MONTEALEGRE, D., and PEARCE, D.A. (2007). Imaging of late infantile neuronal ceroid lipofuscinosis: A clinical rating scale. Neurology 69, 503-504.
25. SKORUPA, A.F., FISHER, K.J., WILSON, J.M., PARENTE, M.K., and WOLFE, J.H. (1999). Sustained production of β-glucuronidase from localized sites after AAV vector gene transfer results in widespread distribution of enzyme and reversal of lysosomal storage lesions in a large volume of brain in mucopolysaccharidosis VII mice. Exp. Neurol. 160, 17-27.
26. SLEAT, D.E., DONNELLY, R.J., LACKLAND, H., LIU, C.G., SOHAR, I., PULLARKAT, R.K., and LOBEL, P. (1997). Association of mutations in a lysosomal protein with classical late-infantile neuronal ceroid lipofuscinosis. Science 277, 1802-1805.
27. SLEAT, D.E., GIN, R.M., SOHAR, I., WISNIEWSKI, K., SKLOWER-BROOKS, S., PULLARKAT, R.K., PALMER, D.N., LERNER, T.J., BOUSTANY, R.M., ULDALL, P., SIAKOTOS, A.N., DONNELLY, R.J., and LOBEL, P. (1999). Mutational analysis of the defective protease in classic late-infantile neuronal ceroid lipofuscinosis, a neurodegenerative lysosomal storage disorder. Am. J. Hum. Genet. 64, 1511-1523.
28. SONDHI, D., HACKETT, N.R., APBLETT, R.L., KAMINSKY, S.M., PERGOLIZZI, R.G., and CRYSTAL, R.G. (2001). Feasibility of gene therapy for late neuronal ceroid lipofuscinosis. Arch. Neurol. 58, 1793-1798.
29. SONDHI, D., PETERSON, D.A., GIANNARIS, E.L., SANDERS, C.T., MENDEZ, B.S., DE, B., ROSTKOWSKI, A.B., BLANCHARD, B., BJUGSTAD, K., SLADEK, J.R., REDMOND, D.E., LEOPOLD, P.L., KAMINSKY, S.M., HACKETT, N.R., and CRYSTAL, R.G. (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.
30. SONDHI, D., HACKETT, N.R., PETERSON, D.A., STRATTON, J., BAAD, M., TRAVIS, K.M., WILSON, J.M., and CRYSTAL, R.G. (2007a). 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.
31. SONDHI, D., HACKETT, N.R., RONDA, J., BAAD, M., and CRYSTAL, R.G. (2007b). Impact of age of treatment on AAVrh.10hCLN2-mediated amelioration of symptoms in CLN2 knockout mouse model of late infantile neuronal ceroid lipofuscinosis. Mol. Ther. 15, S287.
32. STEINFELD, R., HEIM, P., VON GREGORY, H., MEYER, K., ULLRICH, K., GOEBEL, H.H., and KOHLSCHUTTER, A. (2002). Late infantile neuronal ceroid lipofuscinosis: Quantitative description of the clinical course in patients with CLN2 mutations. Am. J. Med. Genet. 112, 347-354.
33. U.S. FOOD AND DRUG ADMINISTRATION. (2003). Meeting 31 of the Biological Response Modifiers Advisory Committee, October 24-26, 2003, Gaithersburg, MD; briefing material and meeting transcripts. Available at www.fda.gov/ohrms/ dockets/ac/cber01.htm#Biological%20Response (accessed April 2008).
34. VINES, D.J., and WARBURTON, M.J. (1999). Classical late infantile neuronal ceroid lipofuscinosis fibroblasts are deficient in lysosomal tripeptidyl peptidase I. FEBS Lett. 443, 131-135.
35. VITE, C.H., PASSINI, M.A., HASKINS, M.E., and WOLFE, J.H. (2003). Adeno-associated virus vector-mediated transduction in the cat brain. Gene Ther. 10, 1874-1881.
36. WILLIAMS, R.E., GOTTLOB, I., LAKE, B.D., GOEBEL, H.H., WINCHESTER, B.G., and WHEELER, R.B. (1999). CLN2: Classic late infantile NCL. In The Neuronal Ceroid Lipofuscinoses (Batten Disease), H.H. Goebel, ed. (Amsterdam: IOS Press), pp. 37-53.
37. WISNIEWSKI, K.E., KIDA, E., GOLABEK, A.A., KACZMARSKI, W., CONNELL, F., and ZHONG, N. (2001). Neuronal ceroid lipofuscinoses: Classification and diagnosis. Adv. Genet. 45, 1-34.
38. WORGALL, S., KEKATPURE, M.V., HEIER, L., BALLON, D., DYKE, J.P., SHUNGU, D., MAO, X., KOSOFSKY, B., KAPLITT, M.G., SOUWEIDANE, M.M., SONDHI, D., HACKETT, N.R., HOLLMANN, C., and CRYSTAL, R.G. (2007). Neurological deterioration in late infantile neuronal ceroid lipofuscinosis. Neurology 69, 521-535.