Systemic AAV9 gene therapy improves the lifespan of mice with Niemann-Pick disease, type C1

Human Molecular Genetics

Volumn 26, Issue 1, 2017, Pages 52-64

  Chandler, Randy J ^a   Williams, Ian M ^b   Gibson, Alana L ^a   Davidson, Cristin D ^c   Incao, Arturo A ^a   Hubbard, Brandon T ^a   Porter, Forbes D ^b   Pavan, William J ^a   Venditti, Charles P ^a  

^a NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; NPC1 PROTEIN, MOUSE; PROTEIN;

ADMINISTRATION AND DOSAGE; ANIMAL; BAGG ALBINO MOUSE; CEREBELLUM; DEPENDOPARVOVIRUS; DISEASE MODEL; FEMALE; GENE THERAPY; GENE VECTOR; GENETICS; KNOCKOUT MOUSE; LONGEVITY; MALE; METABOLISM; MOUSE; NERVE CELL; NIEMANN-PICK DISEASE, TYPE C; PATHOLOGY; PURKINJE CELL;

ANIMALS; CEREBELLUM; CHOLESTEROL; DEPENDOVIRUS; DISEASE MODELS, ANIMAL; FEMALE; GENETIC THERAPY; GENETIC VECTORS; LONGEVITY; MALE; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; NEURONS; NIEMANN-PICK DISEASE, TYPE C; PROTEINS; PURKINJE CELLS;

EID: 85030435525     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddw367     Document Type: Article

References (45)

1. Wassif, C.A., Cross, J.L., Iben, J., Sanchez-Pulido, L., Cougnoux, A., Platt, F.M., Ory, D.S., Ponting, C.P., Bailey-Wilson, J.E., Biesecker, L.G., et al. (2016) High incidence of unrecognized visceral/neurological late-onset Niemann-Pick disease, type C1, predicted by analysis of massively parallel sequencing data sets. Genet. Med., 18, 41-48.
2. Vanier, M.T. (2015) Complex lipid trafficking in Niemann-Pick disease type C. J. Inherit. Metab. Dis., 38, 187-199.
3. Naureckiene, S., Sleat, D.E., Lackland, H., Fensom, A., Vanier, M.T., Wattiaux, R., Jadot, M. and Lobel, P. (2000) Identification of HE1 as the second gene of Niemann-Pick C disease. Science, 290, 2298-2301.
4. Infante, R.E., Radhakrishnan, A., Abi-Mosleh, L., Kinch, L.N., Wang, M.L., Grishin, N.V., Goldstein, J.L. and Brown, M.S. (2008) Purified NPC1 protein: II. Localization of sterol binding to a 240-amino acid soluble luminal loop. J. Biol. Chem., 283, 1064-1075.
5. Wojtanik, K.M. and Liscum, L. (2003) The transport of low density lipoprotein-derived cholesterol to the plasma membrane is defective in NPC1 cells. J. Biol. Chem., 278, 14850-14856.
6. Pentchev, P.G., Comly, M.E., Kruth, H.S., Vanier, M.T., Wenger, D.A., Patel, S. and Brady, R.O. (1985) A defect in cholesterol esterification in Niemann-Pick disease (type C) patients. Proc. Natl Acad. Sci. U S A, 82, 8247-8251.
7. Neufeld, E.B., Cooney, A.M., Pitha, J., Dawidowicz, E.A., Dwyer, N.K., Pentchev, P.G. and Blanchette-Mackie, E.J. (1996) Intracellular trafficking of cholesterol monitored with a cyclodextrin. J. Biol. Chem., 271, 21604-21613.
8. Millard, E.E., Gale, S.E., Dudley, N., Zhang, J., Schaffer, J.E. and Ory, D.S. (2005) The sterol-sensing domain of the Niemann-Pick C1 (NPC1) protein regulates trafficking of low density lipoprotein cholesterol. J. Biol. Chem., 280, 28581-28590.
9. Vanier, M.T., Gissen, P., Bauer, P., Coll, M.J., Burlina, A., Hendriksz, C.J., Latour, P., Goizet, C., Welford, R.W., Marquardt, T., et al. (2016) Diagnostic tests for Niemann-Pick disease type C (NP-C): A critical review. Mol. Genet. Metab., 118:244-254.
10. Patterson, M.C., Hendriksz, C.J., Walterfang, M., Sedel, F., Vanier, M.T. and Wijburg, F. and NP-C Guidelines Working Group. (2012) Recommendations for the diagnosis and management of Niemann-Pick disease type C: an update. Mol. Genet. Metab., 106, 330-344.
11. Patterson, M.C., Mengel, E., Vanier, M.T., Schwierin, B., Muller, A., Cornelisse, P., Pineda, M. and Registry Investigators, N.P.C. (2015) Stable or improved neurological manifestations during miglustat therapy in patients from the international disease registry for Niemann-Pick disease type C: an observational cohort study. Orphanet. J. Rare Dis., 10, 65.
12. Loftus, S.K., Morris, J.A., Carstea, E.D., Gu, J.Z., Cummings, C., Brown, A., Ellison, J., Ohno, K., Rosenfeld, M.A., Tagle, D.A., et al. (1997) Murine model of Niemann-Pick C disease: mutation in a cholesterol homeostasis gene. Science, 277, 232-235.
13. Sarna, J.R., Larouche, M., Marzban, H., Sillitoe, R.V., Rancourt, D.E. and Hawkes, R. (2003) Patterned Purkinje cell degeneration in mouse models of Niemann-Pick type C disease. J. Comp. Neurol., 456, 279-291.
14. Zervas, M., Dobrenis, K. and Walkley, S.U. (2001) Neurons in Niemann-Pick disease type C accumulate gangliosides as well as unesterified cholesterol and undergo dendritic and axonal alterations. J. Neuropathol. Exp. Neurol., 60, 49-64.
15. Loftus, S.K., Erickson, R.P., Walkley, S.U., Bryant, M.A., Incao, A., Heidenreich, R.A. and Pavan, W.J. (2002) Rescue of neurodegeneration in Niemann-Pick C mice by a prion-promoterdriven Npc1 cDNA transgene. Hum. Mol. Genet., 11, 3107-3114.
16. Elrick, M.J., Pacheco, C.D., Yu, T., Dadgar, N., Shakkottai, V.G., Ware, C., Paulson, H.L. and Lieberman, A.P. (2010) Conditional Niemann-Pick C mice demonstrate cell autonomous Purkinje cell neurodegeneration. Hum. Mol. Genet., 19, 837-847.
17. Yu, T., Shakkottai, V.G., Chung, C. and Lieberman, A.P. (2011) Temporal and cell-specific deletion establishes that neuronal Npc1 deficiency is sufficient to mediate neurodegeneration. Hum. Mol. Genet., 20, 4440-4451.
18. Ko, D.C., Milenkovic, L., Beier, S.M., Manuel, H., Buchanan, J. and Scott, M.P. (2005) Cell-autonomous death of cerebellar purkinje neurons with autophagy in Niemann-Pick type C disease. PLoS Genet., 1, 81-95.
19. Foust, K.D., Nurre, E., Montgomery, C.L., Hernandez, A., Chan, C.M. and Kaspar, B.K. (2009) Intravascular AAV9 preferentially targets neonatal neurons and adult astrocytes. Nat. Biotechnol., 27, 59-65.
20. Gray, S.J., Matagne, V., Bachaboina, L., Yadav, S., Ojeda, S.R. and Samulski, R.J. (2011) Preclinical differences of intravascular AAV9 delivery to neurons and glia: a comparative study of adult mice and nonhuman primates. Mol. Ther., 19, 1058-1069.
21. Manfredsson, F.P., Rising, A.C. and Mandel, R.J. (2009) AAV9: a potential blood-brain barrier buster. Mol. Ther., 17, 403-405.
22. McPhee, S.W., Janson, C.G., Li, C., Samulski, R.J., Camp, A.S., Francis, J., Shera, D., Lioutermann, L., Feely, M., Freese, A., et al. (2006) Immune responses to AAV in a phase I study for Canavan disease. J. Gene Med., 8, 577-588.
23. Worgall, S., Sondhi, D., Hackett, N.R., Kosofsky, B., Kekatpure, M.V., Neyzi, N., Dyke, J.P., Ballon, D., Heier, L., Greenwald, B.M., 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.
24. Lein, E.S., Hawrylycz, M.J., Ao, N., Ayres, M., Bensinger, A., Bernard, A., Boe, A.F., Boguski, M.S., Brockway, K.S., Byrnes, E.J., et al. (2007) Genome-wide atlas of gene expression in the adult mouse brain. Nature, 445, 168-176.
25. Pressey, S.N., Smith, D.A., Wong, A.M., Platt, F.M. and Cooper, J.D. (2012) Early glial activation, synaptic changes and axonal pathology in the thalamocortical system of Niemann-Pick type C1 mice. Neurobiol. Dis., 45, 1086-1100.
26. Davidson, C.D., Fishman, Y.I., Puskas, I., Szeman, J., Sohajda, T., McCauliff, L.A., Sikora, J., Storch, J., Vanier, M.T., Szente, L., et al. (2016) Efficacy and ototoxicity of different cyclodextrins in Niemann-Pick C disease. Ann. Clin. Transl. Neurol., 3, 366-380.
27. Foust, K.D., Wang, X., McGovern, V.L., Braun, L., Bevan, A.K., Haidet, A.M., Le, T.T., Morales, P.R., Rich, M.M., Burghes, A.H., et al. (2010) Rescue of the spinal muscular atrophy phenotype in a mouse model by early postnatal delivery of SMN. Nat. Biotechnol., 28, 271-274.
28. Gong, Y., Mu, D., Prabhakar, S., Moser, A., Musolino, P., Ren, J., Breakefield, X.O., Maguire, C.A. and Eichler, F.S. (2015) Adenoassociated virus serotype 9-mediated gene therapy for x-linked adrenoleukodystrophy. Mol. Ther., 23, 824-834.
29. Walia, J.S., Altaleb, N., Bello, A., Kruck, C., LaFave, M.C., Varshney, G.K., Burgess, S.M., Chowdhury, B., Hurlbut, D., Hemming, R., et al. (2015) Long-term correction of Sandhoff disease following intravenous delivery of rAAV9 to mouse neonates. Mol. Ther., 23, 414-422.
30. Passini, M.A., Bu, J., Richards, A.M., Treleaven, C.M., Sullivan, J.A., O'Riordan, C.R., Scaria, A., Kells, A.P., Samaranch, L., San Sebastian, W., et al. (2014) Translational fidelity of intrathecal delivery of self-complementary AAV9-survival motor neuron 1 for spinal muscular atrophy. Hum. Gene Ther., 25, 619-630.
31. Foust, K.D., Salazar, D.L., Likhite, S., Ferraiuolo, L., Ditsworth, D., Ilieva, H., Meyer, K., Schmelzer, L., Braun, L., Cleveland, D.W., et al. (2013) Therapeutic AAV9-mediated suppression of mutant SOD1 slows disease progression and extends survival in models of inherited ALS. Mol. Ther., 21, 2148-2159.
32. Garg, S.K., Lioy, D.T., Cheval, H., McGann, J.C., Bissonnette, J.M., Murtha, M.J., Foust, K.D., Kaspar, B.K., Bird, A. and Mandel, G. (2013) Systemic delivery of MeCP2 rescues behavioral and cellular deficits in female mouse models of Rett syndrome. J. Neurosci., 33, 13612-13620.
33. Nathwani, A.C., Reiss, U.M., Tuddenham, E.G., Rosales, C., Chowdary, P., McIntosh, J., Della Peruta, M., Lheriteau, E., Patel, N., Raj, D., et al. (2014) Long-term safety and efficacy of factor IX gene therapy in hemophilia B. N. Engl J. Med., 371, 1994-2004.
34. Mendell, J.R., Al-Zaidy, S., Shell, R., Arnold, W.D., Rodino-Klapac, L., Kissel, J.T., Prior, T.W., Miranda, C.J., Lowes, L., Alfano, L., et al. (2016), In American Society of Gene and Cell Therapy 19th Annual Meeting, Washington, D.C., in press.
35. Zhang, M., Strnatka, D., Donohue, C., Hallows, J.L., Vincent, I. and Erickson, R.P. (2008) Astrocyte-only Npc1 reduces neuronal cholesterol and triples life span of Npc1-/-mice. J. Neurosci. Res., 86, 2848-2856.
36. Liu, B., Li, H., Repa, J.J., Turley, S.D. and Dietschy, J.M. (2008) Genetic variations and treatments that affect the lifespan of the NPC1 mouse. J. Lipid Res., 49, 663-669.
37. Liu, B., Turley, S.D., Burns, D.K., Miller, A.M., Repa, J.J. and Dietschy, J.M. (2009) Reversal of defective lysosomal transport in NPC disease ameliorates liver dysfunction and neurodegeneration in the npc1-/-mouse. Proc. Natl Acad. Sci. U S A, 106, 2377-2382.
38. Davidson, C.D., Ali, N.F., Micsenyi, M.C., Stephney, G., Renault, S., Dobrenis, K., Ory, D.S., Vanier, M.T. and Walkley, S.U. (2009) Chronic cyclodextrin treatment of murine Niemann-Pick C disease ameliorates neuronal cholesterol and glycosphingolipid storage and disease progression. PLoS One, 4, e6951.
39. Vite, C.H., Bagel, J.H., Swain, G.P., Prociuk, M., Sikora, T.U., Stein, V.M., O'Donnell, P., Ruane, T., Ward, S., Crooks, A., et al. (2015) Intracisternal cyclodextrin prevents cerebellar dysfunction and Purkinje cell death in feline Niemann-Pick type C1 disease. Sci. Transl Med., 7, 276ra226.
40. Pipalia, N.H., Cosner, C.C., Huang, A., Chatterjee, A., Bourbon, P., Farley, N., Helquist, P., Wiest, O. and Maxfield, F.R. (2011) Histone deacetylase inhibitor treatment dramatically reduces cholesterol accumulation in Niemann-Pick type C1 mutant human fibroblasts. Proc. Natl Acad. Sci. U S A, 108, 5620-5625.
41. Alam, M.S., Getz, M. and Haldar, K. (2016) Chronic administration of an HDAC inhibitor treats both neurological and systemic Niemann-Pick type C disease in a mouse model. Sci. Transl Med., 8, 326ra323.
42. Lock, M., Alvira, M., Vandenberghe, L.H., Samanta, A., Toelen, J., Debyser, Z. and Wilson, J.M. (2010) Rapid, simple, and versatile manufacturing of recombinant adenoassociated viral vectors at scale. Hum. Gene Ther., 21, 1259-1271.
43. Williams, I.M., Carletti, B., Leto, K., Magrassi, L. and Rossi, F. (2008) Cerebellar granule cells transplanted in vivo can follow physiological and unusual migratory routes to integrate into the recipient cortex. Neurobiol. Dis., 30, 139-149.
44. Williams, I.M., Wallom, K.L., Smith, D.A., Al Eisa, N., Smith, C. and Platt, F.M. (2014) Improved neuroprotection using miglustat, curcumin and ibuprofen as a triple combination therapy in Niemann-Pick disease type C1 mice. Neurobiol.Dis., 67, 9-17.
45. Millard, E.E., Srivastava, K., Traub, L.M., Schaffer, J.E. and Ory, D.S. (2000) Niemann-pick type C1 (NPC1) overexpression alters cellular cholesterol homeostasis. J. Biol. Chem., 275, 38445-38451.