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

Human Gene Therapy

Volumn 15, Issue 11, 2004, Pages 1131-1154

  Crystal, Ronald G ^a,b   Sondhi, Dolan ^b   Hackett, Neil R ^c   Kaminsky, Stephen M ^c   Worgall, Stefan ^c   Stieg, Philip ^c   Souweidane, Mark ^c   Hosain, Syed ^c   Heier, Linda ^c   Ballon, Douglas ^c   Dinner, Miles ^c   Wisniewski, Krystyna ^d   Kaplitt, Michael ^c   Greenwald, Bruce M ^c   Howell, Joy D ^c   Strybing, Kristin ^c   Dyke, Jonathan ^c   Voss, Henning ^c  

^a WEILL CORNELL MEDICAL CENTER   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c WMC   (United States)

^d NEW YORK STATE INSTITUTE FOR BASIC RESEARCH IN DEVELOPMENTAL DISABILITIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ACTIN; BETA GLOBIN; COMPLEMENTARY DNA; GENE PRODUCT; PARVOVIRUS VECTOR; PEPTIDASE; RECOMBINANT PROTEIN; RECOMBINANT TRIPEPTIDYL PEPTIDASE; SIGNAL PEPTIDE; SINGLE STRANDED DNA; TRIPEPTIDYL PEPTIDASE; UNCLASSIFIED DRUG; PEPTIDE HYDROLASE; PROTEINASE; TRIPEPTIDYL PEPTIDASE I; TRIPEPTIDYL-PEPTIDASE I;

ADENO ASSOCIATED VIRUS; ADENO ASSOCIATED VIRUS SEROTYPE 2; BLOOD CLOTTING DISORDER; BLOOD TOXICITY; CELL LOSS; CHILD DEATH; CHILDHOOD DISEASE; CHRONIC DISEASE; CLINICAL TRIAL; CLN2 GENE; CONFIDENTIALITY; CYTOMEGALOVIRUS; DEGENERATIVE DISEASE; DISEASE SEVERITY; DRUG EFFICACY; ENHANCER REGION; ENZYME DEFICIENCY; ENZYME SYNTHESIS; FEVER; GASTROINTESTINAL SYMPTOM; GENE; GENE CASSETTE; GENE EXPRESSION; GENE MUTATION; GENE THERAPY; GENE TRANSFER; GENETIC DISORDER; GENETIC TRANSCRIPTION; HEALTH CARE PERSONNEL; HUMAN; INTRON; INVERTED TERMINAL REPEAT; KOZAK TRANSLATION INITIATION SIGNAL; LIVER TOXICITY; LYSOSOME STORAGE DISEASE; METHODOLOGY; NEPHROTOXICITY; NEUROLOGIC EXAMINATION; NEURONAL CEROID LIPOFUSCINOSIS; NEURONAL CEROID LIPOFUSCINOSIS LATE INFANTILE TYPE; NEUROTOXICITY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OCCUPATIONAL SAFETY; PATIENT SELECTION; POLYADENYLATION; RATING SCALE; REVIEW; RISK BENEFIT ANALYSIS; SAFETY; SKIN TOXICITY; STOP CODON; TRANSLATION INITIATION; UNITED STATES; VIRUS GENOME; ADOLESCENT; ANIMAL; ARTICLE; BIOLOGICAL MODEL; BRAIN; CERCOPITHECUS; CHILD; GENE VECTOR; GENETICS; GLYCOSYLATION; MALE; METABOLISM; MUTATION; OPEN READING FRAME; PRESCHOOL CHILD; PROSPECTIVE STUDY; RAT; TIME;

ADENO-ASSOCIATED VIRUS; CYTOMEGALOVIRUS; GALLUS GALLUS; HUMAN HERPESVIRUS 5; MIRIDAE; ORYCTOLAGUS CUNICULUS; PARVOVIRUS;

ADOLESCENT; ANIMALS; BRAIN; CERCOPITHECUS AETHIOPS; CHILD; CHILD, PRESCHOOL; DEPENDOVIRUS; DNA, COMPLEMENTARY; ENDOPEPTIDASES; GENE THERAPY; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; GLYCOSYLATION; HUMANS; MALE; MODELS, GENETIC; MUTATION; NEURONAL CEROID-LIPOFUSCINOSES; OPEN READING FRAMES; PEPTIDE HYDROLASES; PROSPECTIVE STUDIES; RATS; TIME FACTORS;

EID: 9244253213     PISSN: 10430342     EISSN: None     Source Type: Journal    
DOI: 10.1089/1043034042431092     Document Type: Review

References (55)

1. AITKEN, M.L., MOSS, R.B., WALTZ, D.A., DOVEY, M.E., TONELLI, M.R., McNAMARA, S.C., GIBSON, R.L., RAMSEY, B.W., CARTER, B.J., and REYNOLDS, T.C. (2001). A phase I study of aerosolized administration of tgAAVCF to cystic fibrosis subjects with mild lung disease. Hum. Gene Ther. 12, 1907-1916.
2. BACKLOW, N.R. (1988). Adeno-associated viruses of human. In: Parvoviruses and Human Disease. Patison, J.R., ed. (CRC Press, Boca Raton, FL) pp. 165-174.
3. BENNETT, J., MAGUIRE, A.M., CIDECIYAN, A.V., SCHNELL, M., GLOVER, E., ANAND, V., ALEMAN, T.S., CHIRMULE, N., GUPTA, A.R., HUANG, Y., GAO, G.P., NYBERG, W.C., TAZELAAR, J., HUGHES, J., WILSON, J.M., and JACOBSON, S.G. (1999). Stable transgene expression in rod photoreceptors after recombinant adeno-associated virus-mediated gene transfer to monkey retina. Proc. Natl. Acad. Sci. U.S.A. 96, 9920-9925.
4. BERNS, K.I., and GIRAUD, C. (1996). Biology of adeno-associated virus. Curr. Top. Microbiol. Immunol. 218, 1-23.
5. BIRCH, D.G. (1999). Retinal degeneration in retinitis pigmentosa and neuronal ceroid lipofuscinosis: An overview. Mol. Genet. Metab. 66, 356-366.
6. 1H-NMR spectroscopic studies of the brain. Neurosci. Biobehav. Rev. 13, 1589-1591.
7. BOSCH, A., PERRET, E., DESMARIS, N., TRONO, D., and HEARD, J.M. (2000). Reversal of pathology in the entire brain of mucopolysaccharidosis type VII mice after lentivirus-mediated gene transfer. Hum. Gene Ther. 11, 1139-1150.
8. BOUSTANY, R.M. (1996). Batten disease or neuronal ceroid lipofuscinosis. In: Neurodystrophies and Neurolipidoses. Moser, H.W., ed. (Elsevier Science, New York) pp. 671-700.
9. CARTER, B. (2000). Adeno-associated virus and adeno-associated virus vectors for gene delivery. In: Gene Therapy. Smyth Tempelton, N., and Lasic, D.D., eds. (Marcel Dekker, New York) pp. 41-59.
10. CHEN, S.J., TAZELAAR, J., MOSCIONI, A.D., and WILSON, J.M. (2000). In vivo selection of hepatocytes transduced with adeno-associated viral vectors. Mol. Ther. 1, 414-422.
11. CHEN, Z.Y., YANT, S.R., HE, C.Y., MEUSE, L., SHEN, S., and KAY, M.A. (2001). Linear DNAs concatemerize in vivo and result in sustained transgene expression in mouse liver. Mol. Ther. 3, 403-410.
12. CHIORINI, J.A., KIM, F., YANG, L., and KOTIN, R.M. (1999). Cloning and characterization of adeno-associated virus type 5. J. Virol. 73, 1309-1319.
13. DAVIDSON, B.L., STEIN, C.S., HETH, J.A., MARTINS, I., KOTIN, R.M., DERKSEN, T.A., ZABNER, J., GHODSI, A., and CHIORINI, J.A. (2000). Recombinant adeno-associated virus type 2, 4, and 5 vectors: Transduction of variant cell types and regions in the mammalian central nervous system. Proc. Natl. Acad. Sci. U.S.A. 97, 3428-3432.
14. DURING, M.J., SAMULSKI, R.J., ELSWORTH, J.D., KAPLITT, M.G., LEONE, P., XIAO, X., LI, J., FREESE, A., TAYLOR, J.R., ROTH, R.H., SLADEK, J.R., JR., O'MALLEY, K.L., and REDMOND, D.E., Jr. (1998). In vivo expression of therapeutic human genes for dopamine production in the caudates of MPTP-treated monkeys using an AAV vector. Gene Ther. 5, 820-827.
15. DURING, M.J., KAPLITT, M.G., STERN, M.B., and EIDELBERG, D. (2001). Subthalamic GAD gene transfer in Parkinson disease patients who are candidates for deep brain stimulation. Hum. Gene Ther. 12, 1589-1591.
16. ELLIGER, S.S., ELLIGER, C.A., AGUILAR, C.P., RAJU, N.R., and WATSON, G.L. (1999). Elimination of lysosomal storage in brains of MPS VII mice treated by intrathecal administration of an adeno-associated virus vector. Gene Ther. 6, 1175-1178.
17. EZAKI, J., WOLFE, L.S., HIGUTI, T., ISHIDOH, K., and KOMINAMI, E. (1995). Specific delay of degradation of mitochondrial ATP synthase subunit c in late infantile neuronal ceroid lipofuscinosis (Batten disease). J. Neurochem. 64, 733-741.
18. FISHER, K.J., JOOSS, K., ALSTON, J., YANG, Y., HAECKER, S.E., HIGH, K., PATHAK, R., RAPER, S.E., and WILSON, J.M. (1997). Recombinant adeno-associated virus for muscle directed gene therapy. Nat. Med. 3, 306-312.
19. FLANNERY, J.G., ZOLOTUKHIN, S., VAQUERO, M.I., LA VAIL, M.M., MUZYCZKA, N., and HAUSWIRTH, W.W. (1997). Efficient photoreceptor-targeted gene expression in vivo by recombinant adeno-associated virus. Proc. Natl. Acad. Sci. U.S.A. 94, 6916-6921.
20. FOOD AND DRUG ADMINISTRATION. 31st Biological Response Modifiers Advisory Committee Meeting, Gaithersburg, MD, October 24, 2003, briefing material and meeting transcripts. Available at URL: http://www.fda.gov/ohrms/dockets/ac/01/ briefing/3794b1.htm.
21. 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.
22. GLADER, B., DAKE, M.D., RAZAVI, M., ZEHNDER, J.L., RUSTAGI, P., HUTCHISON, S., MANNO, C.S., KAYE, R., HERZOG, R.W., ARRUDA, V.R., LEONARD, D., GROSSBARD, E., CHEW, A., COUTO, L., MCCLELLAND, A., JOHNSON, F., HIGH, K.A., and MAY, M.A. A phase I safety study in patients with severe hemophilia B (factor IX deficiency) using adeno-associated viral vector to deliver the gene for human factor IX into the liver. Meeting of the 5th Gene Therapy Workshop, April 12, 2002, Children's Hospital of Philadelphia, Philadelphia, PA. Available at URL: www.hemophilia.org/research/geneabstracts_fri2.htm.
23. HACEIN-BEY-ABINA, S., VON KALLE, C., SCHMIDT, M., MCCORMACK, M.P., WULFFRAAT, N., LEBOULCH, P., LIM, A., OSBORNE, C.S., PAWLIUK, R., MORILLON, E., SORENSEN, R., FORSTER, A., FRASER, P., COHEN, J.I., DE SAINT, B.G., ALEXANDER, I., WINTERGERST, U., FREBOURG, T., AURIAS, A., STOPPA-LYONNET, D., ROMANA, S., RADFORDWEISS, T., GROSS, F., VALENSI, F., DELABESSE, E., MACINTYRE, E., SIGAUX, F., SOULIER, J., LEIVA, L.E., WISSLER, M., PRINZ, C., RABBITTS, T.H., LE DEIST, F., FISCHER, A., and CAVAZZANA-CALVO, M. (2003). LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science 302, 415-419.
24. HASKELL, R.E., HUGHES, S.M., CHIORINI, J.A., ALISKY, J.M., and DAVIDSON, 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.
25. HIGH, K.A. (2001). AAV-mediated gene transfer for hemophilia. Ann. N.Y. Acad. Sci. 953, 64-74.
26. 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). Gene therapy of Canavan disease: AAV-2 vector for neurosurgical delivery of aspartoacylase gene (ASPA) to the human brain [clinical protocol]. Hum. Gene Ther. 13, 1391-1412.
27. KASPAR, B.K., ERICKSON, D., SCHAFFER, D., HINH, L., GAGE, F.H., and PETERSON, D.A. (2002). Targeted retrograde gene delivery for neuronal protection. Mol. Ther. 5, 50-56.
28. KAY, M.A., MANNO, C.S., RAGNI, M.V., LARSON, P.J., COUTO, L.B., MCCLELLAND, A., GLADER, B., CHEW, A.J., TAI, S.J., HERZOG, R.W., ARRUDA, V., JOHNSON, F., SCALLAN, C., SKARSGARD, E., FLAKE, A.W., and HIGH, K.A. (2000). Evidence for gene transfer and expression of factor IX in haemophilia B patients treated with an AAV vector. Nat. Genet. 24, 257-261.
29. KESSLER, P.D., PODSAKOFF, G.M., CHEN, X., MCQUISTON, S.A., COLOSI, P.C., MATELIS, L.A., KURTZMAN, G.J., and BYRNE, B.J. (1996). Gene delivery to skeletal muscle results in sustained expression and systemic delivery of a therapeutic protein. Proc. Natl. Acad. Sci. U.S.A. 93, 14082-14087.
30. KOEBERL, D.D., ALEXANDER, I.E., HALBERT, C.L., RUSSELL, D.W., and MILLER, A.D. (1997). Persistent expression of human clotting factor IX from mouse liver after intravenous injection of adeno-associated virus vectors. Proc. Natl. Acad. Sci. U.S.A. 94, 1426-1431.
31. KURACHI, Y., OKA, A., MIZUGUCHI, M., OHKOSHI, Y., SASAKI, M., ITOH, M., HAYASHI, M., GOTO, Y., and TAKASHIMA, S. (2000). Rapid immunologic diagnosis of classic late infantile neuronal ceroid lipofuscinosis. Neurology 54, 1676-1680.
32. LEONE, P., and SIMEONE, F.A. (2000). Gene therapy of Canavan disease using AAV for brain gene transfer. RAC 381-(2000-01). Available at URL http://www4.od.nih.gov/oba/rac/trialquery.asp?C2=3&piid=5509.
33. LIN, L., and LOBEL, P. (2001). Production and characterization of recombinant human CLN2 protein for enzyme-replacement therapy in late infantile neuronal ceroid lipofuscinosis. Biochem. J. 357, 49-55.
34. LIU, C.G., SLEAT, D.E., DONNELLY, R.J., and LOBEL, P. (1998). Structural organization and sequence of CLN2, the defective gene in classical late infantile neuronal ceroid lipofuscinosis. Genomics 50, 206-212.
35. LO, W.D., QU, G., SFERRA, T.J., CLARK, R., CHEN, R., and JOHNSON, P.R. (1999). Adeno-associated virus-mediated gene transfer to the brain: Duration and modulation of expression. Hum. Gene Ther. 10, 201-213.
36. LODISH, H., BERK, A., ZIPURSKY, S.L., MATSUDAIRA, P., BALTIMORE, D., and DARNELL, J. (2000). Protein sorting: Organelle biogenesis and protein secretion. In: Molecular Cell Biology. (W.H. Freeman and Company, New York) pp. 677-751.
37. MAEDA, Y., IKEDA, U., SHIMPO, M., UENO, S., OGASAWARA, Y., URABE, M., KUME, A., TAKIZAWA, T., SAITO, T., COLOSI, P., KURTZMAN, G., SHIMADA, K., and OZAWA, K. (1998). Efficient gene transfer into cardiac myocytes using adeno-associated virus (AAV) vectors. J. Mol. Cell. Cardiol. 30, 1341-1348.
38. MANDEL, R.J., RENDAHL, K.G., SPRATT, S.K., SNYDER, R.O., COHEN, L.K., and LEFF, S.E. (1998). Characterization of intrastriatal recombinant adeno-associated virus-mediated gene transfer of human tyrosine hydroxylase and human GTP-cyclohydrolase I in a rat model of Parkinson's disease. J. Neurosci. 18, 4271-4284.
39. MCCORMACK, M.P., and RABBITTS, T.H. (2004). Activation of the T-cell oncogene LMO2 after gene therapy for X-linked severe combined immunodeficiency. N. Engl. J. Med. 350, 913-922.
40. MCCOWN, T.J., XIAO, X., LI, J., BREESE, G.R., and SAMULSKI, R.J. (1996). Differential and persistent expression patterns of CNS gene transfer by an adeno-associated virus (AAV) vector. Brain Res. 713, 99-107.
41. MOLE, S.E. (1999). Batten's disease: Eight genes and still counting? Lancet 354, 443-445.
42. MUZYCZKA, N. (1992). Use of adeno-associated virus as a general transduction vector for mammalian cells. Curr. Top. Microbiol. Immunol. 158, 97-129.
43. NEW YORK PRESBYTERIAN HOSPITAL-WEILL MEDICAL COLLEGE OF CORNELL UNIVERSITY CHILDREN'S CLINICAL RESEARCH CENTER. Clinical Testing Guidelines, Blood Drawing Sheet. August 26, 2003. URL: http://ccrc.med.cornell.edu/ patsafety/bloodvol/blooddrawingsheet.pdf
44. PATERNA, J.C., MOCCETTI, T., MURA, A., FELDON, J., and BUELER, H. (2000). Influence of promoter and WHV post-transcriptional regulatory element on AAV-mediated transgene expression in the rat brain. Gene Ther. 7, 1304-1311.
45. PELTONEN, L., SAVUKOSKI, M., and VESA, J. (2000). Genetics of the neuronal ceroid lipofuscinoses. Curr. Opin. Genet. Dev. 10, 299-305.
46. PURANAM, K., QIAN, W.H., NIKBAKHT, K., VENABLE, M., OBEID, L., HANNUN, Y., and BOUSTANY, R.M. (1997). Upregulation of Bcl-2 and elevation of ceramide in Batten disease. Neuropediatrics 28, 37-41.
47. SFERRA, T.J., QU, G., McNEELY, D., RENNARD, R., CLARK, K.R., LO, W.D., and JOHNSON, P.R. (2000). Recombinant adeno-associated virus-mediated correction of lysosomal storage within the central nervous system of the adult mucopolysaccharidosis type VII mouse. Hum. Gene Ther. 11, 507-519.
48. SHARP, J.D., WHEELER, R.B., LAKE, B.D., SAVUKOSKI, M., JARVELA, I.E., PELTONEN, L., GARDINER, R.M., and WILLIAMS, R.E. (1997). Loci for classical and a variant late infantile neuronal ceroid lipofuscinosis map to chromosomes 11p15 and 15q21-23. Hum. Mol. Genet. 6, 591-595.
49. 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.
50. 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.
51. SLEAT, D.E., GIN, R.M., SOHAR, I., WISNIEWSKI, K., SKLOWERBROOKS, 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.
52. 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.
53. 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.
54. WAGNER, J.A., MORAN, M.L., MESSNER, A.H., DAIFUKU, R., CONRAD, C.K., REYNOLDS, T., GUGGINO, W.B., MOSS, R.B., CARTER, B.J., WINE, J.J., FLOTTE, T.R., and GARDNER, P. (1998). A phase I/II study of tgAAV-CF for the treatment of chronic sinusitis in patients with cystic fibrosis. Hum. Gene Ther. 9, 889-909.
55. WILLIAMS, R.E., GOTTLOB, I., LAKE, B.D., GOEBEL, H.H., WINCHESTER, B.G., and WHEELER, R.B. (1999). CLN 2. Classic late infantile NCL. In: The Neuronal Ceroid Lipofuscinoses (Batten Disease). Goebel, H.H., Mole, S.E., and Lake, B.D., eds. (IOS Press, Amsterdam) pp. 37-54.