CNS-targeted AAV5 gene transfer results in global dispersal of vector and prevention of morphological and function deterioration in CNS of globoid cell leukodystrophy mouse model

Molecular Genetics and Metabolism

Volumn 103, Issue 4, 2011, Pages 367-377

  Lin, Dar Shong ^a,b,d   Hsiao, Chung Der ^e   Liau, Ian ^f   Lin, Shuan Pei ^a,b   Chiang, Ming Fu ^a,c   Chuang, Chih Kuang ^a,d   Wang, Tuen Jen ^a   Wu, Tsu Yen ^a   Jian, Yuan Ren ^a   Huang, Sung Fa ^a   Liu, Hsuan Liang ^d  

^a MACKAY MEMORIAL HOSPITAL   (Taiwan)

^b NURSING AND MANAGEMENT COLLEGE   (Taiwan)

^c TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^d NATIONAL TAIPEI UNIVERSITY OF TECHNOLOGY   (Taiwan)

^e CHUNG YUAN CHRISTIAN UNIVERSITY   (Taiwan)

^f NATIONAL CHIAO TUNG UNIVERSITY   (Taiwan)

Author keywords

Adeno associated virus; Globoid cell leukodystrophy; Lysosomal storage disease; Purkinje cells

Indexed keywords

CALBINDIN; GALACTOSYLCERAMIDASE; PSYCHOSINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROTECTION; CELL SURVIVAL; CENTRAL NERVOUS SYSTEM; CEREBELLUM; CONTROLLED STUDY; DEMYELINATING DISEASE; DRUG TARGETING; ENZYME DEFICIENCY; GENE TARGETING; GLIOSIS; GLOBOID CELL LEUKODYSTROPHY; HIPPOCAMPUS; HISTOPATHOLOGY; LIFESPAN; LUMBAR SPINAL CORD; MOTONEURON; MOUSE; NEOCORTEX; NERVE FIBER; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PURKINJE CELL; SPINAL CORD; THALAMUS; TRANSGENE; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY;

ANIMALS; BRAIN; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; DEPENDOVIRUS; DISEASE MODELS, ANIMAL; GALACTOSYLCERAMIDASE; GENE THERAPY; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; IMMUNOHISTOCHEMISTRY; LEUKODYSTROPHY, GLOBOID CELL; MICE; MICE, TRANSGENIC; SPINAL CORD;

ADENO-ASSOCIATED VIRUS; MURINAE; MUS;

EID: 79960840654     PISSN: 10967192     EISSN: 10967206     Source Type: Journal    
DOI: 10.1016/j.ymgme.2011.05.005     Document Type: Article

References (47)

1. Suzuki K., Suzuki Y. Globoid cell leucodystrophy (Krabbe's disease): deficiency of galactocerebroside beta-galactosidase. Proc. Natl. Acad. Sci. U.S.A. 1970, 66:302-309.
2. Wenger D.A., Rafi M.A., Luzi P. Molecular genetics of Krabbe disease (globoid cell leukodystrophy): diagnostic and clinical implications. Hum. Mutat. 1997, 10:268-279.
3. Suzuki K., Taniike M. Murine model of genetic demyelinating disease: the twitcher mouse. Microsc. Res. Technol. 1995, 32:204-214.
4. Suzuki K., Hoogerbrugge P.M., Poorthuis B.J., Bekkum D.W. The twitcher mouse. Central nervous system pathology after bone marrow transplantation. Lab. Invest. 1988, 58:302-309.
5. Duffner P.K., Caviness V.S., Erbe R.W., Patterson M.C., Schultz K.R., Wenger D.A., Whitley C. The long-term outcomes of presymptomatic infants transplanted for Krabbe disease: report of the workshop held on July 11 and 12, 2008, Holiday Valley, New York. Genet. Med. 2009, 11:450-454.
6. Sands M.S., Davidson B.L. Gene therapy for lysosomal storage diseases. Mol. Ther. 2006, 13:839-849.
7. Shen J.S., Watabe K., Ohashi T., Eto Y. Intraventricular administration of recombinant adenovirus to neonatal twitcher mouse leads to clinicopathological improvements. Gene Ther. 2001, 8:1081-1087.
8. Rafi M.A., Zhi Rao H., Passini M.A., Curtis M., Vanier M.T., Zaka M., Luzi P., Wolfe J.H., Wenger D.A. AAV-mediated expression of galactocerebrosidase in brain results in attenuated symptoms and extended life span in murine models of globoid cell leukodystrophy. Mol. Ther. 2005, 11:734-744.
9. Lin D., Fantz C.R., Levy B., Rafi M.A., Vogler C., Wenger D.A., Sands M.S. AAV2/5 vector expressing galactocerebrosidase ameliorates CNS disease in the murine model of globoid-cell leukodystrophy more efficiently than AAV2. Mol. Ther. 2005, 12:422-430.
10. Lattanzi A., Neri M., Maderna C., di Girolamo I., Martino S., Orlacchio A., Amendola M., Naldini L., Gritti A. Widespread enzymatic correction of CNS tissues by a single intracerebral injection of therapeutic lentiviral vector in leukodystrophy mouse models. Hum. Mol. Genet. 2010, 19:2208-2227.
11. Lin D., Donsante A., Macauley S., Levy B., Vogler C., Sands M.S. Central nervous system-directed AAV2/5-mediated gene therapy synergizes with bone marrow transplantation in the murine model of globoid-cell leukodystrophy. Mol. Ther. 2007, 15:44-52.
12. Galbiati F., Givogri M.I., Cantuti L., Rosas A.L., Cao H., van Breemen R., Bongarzone E.R. Combined hematopoietic and lentiviral gene-transfer therapies in newborn Twitcher mice reveal contemporaneous neurodegeneration and demyelination in Krabbe disease. J. Neurosci. Res. 2009, 87:1748-1759.
13. Sakai N., Inui K., Tatsumi N., Fukushima H., Nishigaki T., Taniike M., Nishimoto J., Tsukamoto H., Yanagihara I., Ozono K., Okada S. Molecular cloning and expression of cDNA for murine galactocerebrosidase and mutation analysis of the twitcher mouse, a model of Krabbe's disease. J. Neurochem. 1996, 66:1118-1124.
14. Wenger D.A., Williams C. Screening for lysosomal disorders. Techniques in Diagnostics Human Biochemical Genetics 1991, 587-617. Wiley-Liss, New York. F.A. Hommes (Ed.).
15. Lee W.C., Courtenay A., Troendle F.J., Stallings-Mann M.L., Dickey C.A., DeLucia M.W., Dickson D.W., Eckman C.B. Enzyme replacement therapy results in substantial improvements in early clinical phenotype in a mouse model of globoid cell leukodystrophy. FASEB J. 2005, 19:1549-1551.
16. Dolcetta D., Perani L., Givogri M.I., Galbiati F., Orlacchio A., Martino S., Roncarolo M.G., Bongarzone E. Analysis of galactocerebrosidase activity in the mouse brain by a new histological staining method. J. Neurosci. Res. 2004, 77:462-464.
17. Ida H., Rennert O.M., Watabe K., Eto Y., Maekawa K. Pathological and biochemical studies of fetal Krabbe disease. Brain Dev. 1994, 16:480-484.
18. LeVine S.M., Wetzel D.L., Eilert A.J. Neuropathology of twitcher mice: examination by histochemistry, immunohistochemistry, lectin histochemistry and Fourier transform infrared microspectroscopy. Int. J. Dev. Neurosci. 1994, 12:275-288.
19. Taniike M., Suzuki K. Spacio-temporal progression of demyelination in twitcher mouse: with clinico-pathological correlation. Acta Neuropathol. 1994, 88:228-236.
20. Mikoshiba K., Fujishiro M., Kohsaka S., Okano H., Takamatsu K., Tsukada Y. Disorders in myelination in the twitcher mutant: immunohistochemical and biochemical studies. Neurochem. Res. 1985, 10:1129-1141.
21. Griffey M., Macauley S.L., Ogilvie J.M., Sands M.S. AAV2-mediated ocular gene therapy for infantile neuronal ceroid lipofuscinosis. Mol. Ther. 2005, 12:413-421.
22. Cearley C.N., Wolfe J.H. A single injection of an adeno-associated virus vector into nuclei with divergent connections results in widespread vector distribution in the brain and global correction of a neurogenetic disease. J. Neurosci. 2007, 27:9928-9940.
23. Dodge J.C., Clarke J., Song A., Bu J., Yang W., Taksir T.V., Griffiths D., Zhao M.A., Schuchman E.H., Cheng S.H., O'Riordan C.R., Shihabuddin L.S., Passini M.A., Stewart G.R. Gene transfer of human acid sphingomyelinase corrects neuropathology and motor deficits in a mouse model of Niemann-Pick type A disease. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:17822-17827.
24. 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., Crystal R.G. Intracranial delivery of CLN2 reduces brain pathology in a mouse model of classical late infantile neuronal ceroid lipofuscinosis. J. Neurosci. 2006, 26:1334-1342.
25. Tanaka Y., Okado H., Terashima T. Retrograde infection of precerebellar nuclei neurons by injection of a recombinant adenovirus into the cerebellar cortex of normal and reeler mice. Arch. Histol. Cytol. 2007, 70:51-62.
26. Broekman M.L., Tierney L.A., Benn C., Chawla P., Cha J.H., Sena-Esteves M. Mechanisms of distribution of mouse beta-galactosidase in the adult GM1-gangliosidosis brain. Gene Ther. 2009, 16:303-308.
27. Berges B.K., Yellayi S., Karolewski B.A., Miselis R.R., Wolfe J.H., Fraser N.W. Widespread correction of lysosomal storage in the mucopolysaccharidosis type VII mouse brain with a herpes simplex virus type 1 vector expressing beta-glucuronidase. Mol. Ther. 2006, 13:859-869.
28. Giannetti S., Molinari M. Cerebellar input to the posterior parietal cortex in the rat. Brain Res. Bull. 2002, 58:481-489.
29. Ruigrok T.J., Pijpers A., Goedknegt-Sabel E., Coulon P. Multiple cerebellar zones are involved in the control of individual muscles: a retrograde transneuronal tracing study with rabies virus in the rat. Eur. J. Neurosci. 2008, 28:181-200.
30. Sondhi D., Peterson D.A., Edelstein A.M., del Fierro K., Hackett N.R., Crystal R.G. Survival advantage of neonatal CNS gene transfer for late infantile neuronal ceroid lipofuscinosis. Exp. Neurol. 2008, 213:18-27.
31. Passini M.A., Wolfe J.H. Widespread gene delivery and structure-specific patterns of expression in the brain after intraventricular injections of neonatal mice with an adeno-associated virus vector. J. Virol. 2001, 75:12382-12392.
32. Passini M.A., Watson D.J., Vite C.H., Landsburg D.J., Feigenbaum A.L., Wolfe J.H. Intraventricular brain injection of adeno-associated virus type 1 (AAV1) in neonatal mice results in complementary patterns of neuronal transduction to AAV2 and total long-term correction of storage lesions in the brains of beta-glucuronidase-deficient mice. J. Virol. 2003, 77:7034-7040.
33. Colle M.A., Piguet F., Bertrand L., Raoul S., Bieche I., Dubreil L., Sloothaak D., Bouquet C., Moullier P., Aubourg P., Cherel Y., Cartier N., Sevin C. Efficient intracerebral delivery of AAV5 vector encoding human ARSA in non-human primate. Hum. Mol. Genet. 2010, 19:147-158.
34. Bae J.S., Furuya S., Shinoda Y., Endo S., Schuchman E.H., Hirabayashi Y., Jin H.K. Neurodegeneration augments the ability of bone marrow-derived mesenchymal stem cells to fuse with Purkinje neurons in Niemann-Pick type C mice. Hum. Gene Ther. 2005, 16:1006-1011.
35. Torashima T., Koyama C., Iizuka A., Mitsumura K., Takayama K., Yanagi S., Oue M., Yamaguchi H., Hirai H. Lentivector-mediated rescue from cerebellar ataxia in a mouse model of spinocerebellar ataxia. EMBO Rep. 2008, 9:393-399.
36. Sevin C., Benraiss A., Van Dam D., Bonnin D., Nagels G., Verot L., Laurendeau I., Vidaud M., Gieselmann V., Vanier M., De Deyn P.P., Aubourg P., Cartier N. Intracerebral adeno-associated virus-mediated gene transfer in rapidly progressive forms of metachromatic leukodystrophy. Hum. Mol. Genet. 2006, 15:53-64.
37. Strazza M., Luddi A., Carbone M., Rafi M.A., Costantino-Ceccarini E., Wenger D.A. Significant correction of pathology in brains of twitcher mice following injection of genetically modified mouse neural progenitor cells. Mol. Genet. Metab. 2009, 97:27-34.
38. Luddi A., Volterrani M., Strazza M., Smorlesi A., Rafi M.A., Datto J., Wenger D.A., Costantino-Ceccarini E. Retrovirus-mediated gene transfer and galactocerebrosidase uptake into twitcher glial cells results in appropriate localization and phenotype correction. Neurobiol. Dis. 2001, 8:600-610.
39. Jeyakumar M., Dwek R.A., Butters T.D., Platt F.M. Storage solutions: treating lysosomal disorders of the brain. Nat. Rev. Neurosci. 2005, 6:713-725.
40. Cachon-Gonzalez M.B., Wang S.Z., Lynch A., Ziegler R., Cheng S.H., Cox T.M. Effective gene therapy in an authentic model of Tay-Sachs-related diseases. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:10373-10378.
41. Zhong L., Li B., Mah C.S., Govindasamy L., Agbandje-McKenna M., Cooper M., Herzog R.W., Zolotukhin I., Warrington K.H., Weigel-Van Aken K.A., Hobbs J.A., Zolotukhin S., Muzyczka N., Srivastava A. Next generation of adeno-associated virus 2 vectors: point mutations in tyrosines lead to high-efficiency transduction at lower doses. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:7827-7832.
42. Davidson B.L., Stein C.S., Heth J.A., Martins I., Kotin R.M., Derksen T.A., Zabner J., Ghodsi A., Chiorini J.A. 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. 2000, 97:3428-3432.
43. Watson D.J., Passini M.A., Wolfe J.H. Transduction of the choroid plexus and ependyma in neonatal mouse brain by vesicular stomatitis virus glycoprotein-pseudotyped lentivirus and adeno-associated virus type 5 vectors. Hum. Gene Ther. 2005, 16:49-56.
44. 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., Passini M.A. Timing of therapeutic intervention determines functional and survival outcomes in a mouse model of late infantile Batten disease. Mol. Ther. 2007, 15:1782-1788.
45. Gasbarri A., Pompili A., Pacitti C., Cicirata F. Comparative effects of lesions to the ponto-cerebellar and olivo-cerebellar pathways on motor and spatial learning in the rat. Neuroscience 2003, 116:1131-1140.
46. Galbiati F., Basso V., Cantuti L., Givogri M.I., Lopez-Rosas A., Perez N., Vasu C., Cao H., van Breemen R., Mondino A., Bongarzone E.R. Autonomic denervation of lymphoid organs leads to epigenetic immune atrophy in a mouse model of Krabbe disease. J. Neurosci. 2007, 27:13730-13738.
47. White A.B., Givogri M.I., Lopez-Rosas A., Cao H., van Breemen R., Thinakaran G., Bongarzone E.R. Psychosine accumulates in membrane microdomains in the brain of krabbe patients, disrupting the raft architecture. J. Neurosci. 2009, 29:6068-6077.