Adeno-associated virus-mediated expression of β-hexosaminidase prevents neuronal loss in the sandhoff mouse brain

Human Molecular Genetics

Volumn 20, Issue 22, 2011, Pages 4371-4380

  Sargeant, Timothy J ^a   Wang, Susan ^a   Bradley, Josephine ^a   Smith, Nicolas J C ^a   Raha, Animesh A ^a   McNair, Rosamund ^a   Ziegler, Robin J ^b   Cheng, Seng H ^b   Cox, Timothy M ^a   Cachón González, Maria Begoña ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b GENZYME CORPORATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA N ACETYLHEXOSAMINIDASE A; BETA N ACETYLHEXOSAMINIDASE B; NEURON SPECIFIC NUCLEAR PROTEIN; PARVOVIRUS VECTOR;

AGE DISTRIBUTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN NERVE CELL; CELL DENSITY; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; FACIAL NERVE NUCLEUS; FEMALE; GENE TRANSFER; LATERAL VESTIBULAR NUCLEUS; MALE; MOUSE; NERVE CELL NECROSIS; NICK END LABELING; NONHUMAN; PRIMARY MOTOR CORTEX; PRIMARY SOMATOSENSORY CORTEX; PRIORITY JOURNAL; PURKINJE CELL; SANDHOFF DISEASE; SPINAL CORD NERVE CELL; SPINAL CORD VENTRAL HORN; THALAMUS LATERAL NUCLEUS; THALAMUS VENTRAL NUCLEUS; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY;

ANIMALS; APOPTOSIS; BETA-N-ACETYLHEXOSAMINIDASES; BRAIN; DEPENDOVIRUS; GENETIC VECTORS; IN SITU NICK-END LABELING; MICE; NEURONS; SANDHOFF DISEASE;

ADENO-ASSOCIATED VIRUS; ANIMALIA; MURINAE; MUS;

EID: 80054916282     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddr364     Document Type: Article

References (43)

1. Tay, W. (1881) Symmetrical changes in the region of the yellow spot in each eye of an infant. Trans. Opthal. Soc., 1, 55-57.
2. Sachs, B. (1887) On arrested cerebral development with special reference to cortical pathology. J. Nerv. Ment. Dis., 14, 541-554.
3. Sandhoff, K., Andreae, U. and Jatzkewitz, H. (1968) Deficient hexosaminidase activity in an exceptional case of Tay-Sachs disease with additional storage of kidney globoside in visceral organs. Life Sci., 7, 283-288.
4. Conzelmann, E. and Sandhoff, K. (1978) AB variant of infantile GM2 gangliosidosis: deficiency of a factor necessary for stimulation of hexosaminidase A-catalyzed degradation of ganglioside GM2 and glycolipid GA2. Proc. Natl Acad. Sci. USA, 75, 3979-3983.
5. Svennerholm, L. (1962) The chemical structure of normal human brain and Tay-Sachs gangliosides. Biochem. Biophys. Res. Commun., 9, 436-441.
6. Makita, A. and Yamakawa, T. (1963) The glycolipids of the brain of Tay-Sachs' disease. The chemical structures of globoside and main ganglioside. Jpn. J. Exp. Med., 33, 361-368.
7. Ledeen, R. and Salsman, K. (1965) Structure of the Tay-Sachs' ganglioside. Biochemistry, 4, 2225-2233.
8. Sango, K., Yamanaka, S., Hoffmann, A., Okuda, Y., Grinberg, A., Westphal, H., McDonald, M.P., Crawley, J.N., Sandhoff, K., Suzuki, K. et al. (1995) Mouse models of Tay-Sachs and Sandhoff diseases differ in neurologic phenotype and ganglioside metabolism. Nat. Genet., 11, 170-176.
9. Jeyakumar, M., Thomas, R., Elliot-Smith, E., Smith, D.A., van der Spoel, A.C., d'Azzo, A., Perry, V.H., Butters, T.D., Dwek, R.A. and Platt, F.M. (2003) Central nervous system inflammation is a hallmark of pathogenesis in mouse models of GM1 and GM2 gangliosidosis. Brain, 126, 974-987.
10. Huang, J.-Q., Trasler, J.M., Igdoura, S., Michaud, J., Hanai, N. and Gravel, R.A. (1997) Apoptotic cell death in mouse models of GM2 gangliosidosis and observations on human Tay-Sachs and Sandhoff diseases. Hum. Mol. Genet., 6, 1879-1885.
11. Wada, R., Tifft, C.J. and Proia, R.L. (2000) Microglial activation precedes acute neurodegeneration in Sandhoff disease and is suppressed by bone marrow transplantation. Proc. Natl Acad. Sci. USA, 97, 10954-10959.
12. Volk, B.W. (1964) Pathologic anatomy. In: Volk, B.W. (ed.), Tay-Sachs' Disease. Grune and Stratton, Inc., New York, USA, pp. 36-67.
13. Cachón-González, M.B., Wang, S.Z., Lynch, A., Ziegler, R., Cheng, S.H. and Cox, T.M. (2006) Effective gene therapy in an authentic model of Tay-Sachs-related diseases. Proc. Natl Acad. Sci. USA, 103, 10373-10378.
14. Jeyakumar, M., Smith, D.A., Williams, I.M., Borja, M.C., Neville, D.C., Butters, T.D., Dwek, R.A. and Platt, F.M. (2004) NSAIDs increase survival in the Sandhoff disease mouse: synergy with N-butyldeoxynojirimycin. Ann. Neurol., 56, 624-629.
15. Lee, J.P., Jeyakumar, M., Gonzalez, R., Takahashi, H., Lee, P.J., Baek, R.C., Clark, D., Rose, H., Fu, G., Clarke, J. et al. (2007) Stem cells act through multiple mechanisms to benefit mice with neurodegenerative metabolic disease. Nat. Med., 13, 439-447.
16. Norflus, F., Tifft, C.J., McDonald, M.P., Goldstein, G., Crawley, J.N., Hoffmann, A., Sandhoff, K., Suzuki, K. and Proia, R.L. (1998) Bone marrow transplantation prolongs life span and ameliorates neurologic manifestations in Sandhoff disease mice. J. Clin. Invest., 101, 1881-1888.
17. Hickman, S., Shapiro, L.J. and Neufeld, E.F. (1974) A recognition marker required for uptake of a lysosomal enzyme by cultured fibroblasts. Biochem. Biophys. Res. Commun., 57, 55-61.
18. Lopez, M.E., Klein, A.D., Dimbil, U.J. and Scott, M.P. (2011) Anatomically defined neuron-based rescue of neurodegenerative Niemann-Pick type C disorder. J. Neurosci., 31, 4367-4378.
19. Hu, Z., Yuri, K., Ozawa, H., Lu, H. and Kawata, M. (1997) The in vivo time course for elimination of adrenalectomy-induced apoptotic profiles from the granule cell layer of the rat hippocampus. J. Neurosci., 17, 3981-3989.
20. Venkatachalam, K., Long, A.A., Elsaesser, R., Nikolaeva, D., Broadie, K. and Montell, C. (2008) Motor deficit in a Drosophila model of mucolipidosis type IV due to defective clearance of apoptotic cells. Cell, 135, 838-851.
21. Kao, A.W., Eisenhut, R.J., Martens, L.H., Nakamura, A., Huang, A., Bagley, J.A., Zhou, P., de Luis, A., Neukomm, L.J., Cabello, J. et al. (2011) A neurodegenerative disease mutation that accelerates the clearance of apoptotic cells. Proc. Natl Acad. Sci. USA, 108, 4441-4446.
22. Kay, G.W., Jay, N.P. and Palmer, D.N. (2011) The specific loss of GnRH-positive neurons from the hypothalamus of sheep with CLN6 neuronal ceroid lipofuscinosis occurs without glial activation and has only minor effects on reproduction. Neurobiol. Dis., 41, 614-623.
23. von Lewinski, F. and Keller, B.U. (2005) Ca2+, mitochondria and selective motoneuron vulnerability: implications for ALS. Trends Neurosci., 28, 494-500.
24. Brustovetsky, N., Brustovetsky, T., Purl, K.J., Capano, M., Crompton, M. and Dubinsky, J.M. (2003) Increased susceptibility of striatal mitochondria to calcium-induced permeability transition. J. Neurosci., 23, 4858-4867.
25. Yamada, A., Saji, M., Ukita, Y., Shinoda, Y., Taniguchi, M., Higaki, K., Ninomiya, H. and Ohno, K. (2001) Progressive neuronal loss in the ventral posterior lateral and medial nuclei of thalamus in Niemann-Pick disease type C mouse brain. Brain Dev., 23, 288-297.
26. Kielar, C., Maddox, L., Bible, E., Pontikis, C.C., Macauley, S.L., Griffey, M.A., Wong, M., Sands, M.S. and Cooper, J.D. (2007) Successive neuron loss in the thalamus and cortex in a mouse model of infantile neuronal ceroid lipofuscinosis. Neurobiol. Dis., 25, 150-162.
27. Enquist, I.B., Lo Bianco, C., Ooka, A., Nilsson, E., Månsson, J.E., Ehinger, M., Richter, J., Brady, R.O., Kirik, D. and Karlsson, S. (2007) Murine models of acute neuronopathic Gaucher disease. Proc. Natl Acad. Sci. USA, 104, 17483-17488.
28. Farfel-Becker, T., Vitner, E.B., Pressey, S.N., Eilam, R., Cooper, J.D. and Futerman, A.H. (2011) Spatial and temporal correlation between neuron loss and neuroinflammation in a mouse model of neuronopathic Gaucher disease. Hum. Mol. Genet., 20, 1375-1386.
29. 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.
30. Francis, J.T., Xu, S. and Chapin, J.K. (2008) Proprioceptive and cutaneous representations in the rat ventral posterolateral thalamus. J. Neurophysiol., 99, 2291-2304.
31. Terashima, T., Oka, K., Kritz, A.B., Kojima, H., Baker, A.H. and Chan, L. (2009) DRG-targeted helper-dependent adenoviruses mediate selective gene delivery for therapeutic rescue of sensory neuronopathies in mice. J. Clin. Invest., 119, 2100-2112.
32. Ruigrok, T.J., Pijpers, A., Goedknegt-Sabel, E. and Coulon, P. (2008) 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., 28, 181-200.
33. Walkley, S.U., Baker, H.J., Rattazzi, M.C., Haskins, M.E. and Wu, J.Y. (1991) Neuroaxonal dystrophy in neuronal storage disorders: evidence for major GABAergic neuron involvement. J. Neurol. Sci., 104, 1-8.
34. Walkley, S.U., Sikora, J., Micsenyi, M., Davidson, C. and Dobrenis, K. (2010) Lysosomal compromise and brain dysfunction: examining the role of neuroaxonal dystrophy. Biochem. Soc. Trans., 38, 1436-1441.
35. Phaneuf, D., Wakamatsu, N., Huang, J.Q., Borowski, A., Peterson, A.C., Fortunato, S.R., Ritter, G., Igdoura, S.A., Morales, C.R., Benoit, G. et al. (1996) Dramatically different phenotypes in mouse models of human Tay-Sachs and Sandhoff diseases. Hum. Mol. Genet., 5, 1-14.
36. McNally, M.A., Baek, R.C., Avila, R.L., Seyfried, T.N., Strichartz, G.R. and Kirschner, D.A. (2007) Peripheral nervous system manifestations in a Sandhoff disease mouse model: nerve conduction, myelin structure, lipid analysis. J. Negat. Results Biomed., 6, 8.
37. Baek, R.C., Martin, D.R., Cox, N.R. and Seyfried, T.N. (2009) Comparative analysis of brain lipids in mice, cats, and humans with Sandhoff disease. Lipids, 44, 197-205.
38. Kolodny, E.H., Kanfer, J., Quirk, J.M. and Brady, R.O. (1971) Properties of a particle-bound enzyme from rat intestine that cleaves sialic acid from Tay-Sachs ganglioside. J. Biol. Chem., 246, 1426-1431.
39. Ginzburg, L., Li, S.C., Li, Y.T. and Futerman, A.H. (2008) An exposed carboxyl group on sialic acid is essential for gangliosides to inhibit calcium uptake via the sarco/endoplasmic reticulum Ca2+-ATPase: relevance to gangliosidoses. J. Neurochem., 104, 140-146.
40. Ginzburg, L., Kacher, Y. and Futerman, A.H. (2004) The pathogenesis of glycosphingolipid storage disorders. Semin. Cell Dev. Biol., 15, 417-431.
41. Colussi-Mas, J., Geisler, S., Zimmer, L., Zahm, D.S. and Berod, A. (2007) Activation of afferents to the ventral tegmental area in response to acute amphetamine: a double-labelling study. Eur. J. Neurosci., 26, 1011-1025.
42. Hudson, A.J., Kiernan, J.A., Munoz, D.G., Pringle, C.E., Brown, W.F. and Ebers, G.C. (1993) Clinicopathological features of primary lateral sclerosis are different from amyotrophic lateral sclerosis. Brain Res. Bull., 30, 359-364.
43. Molon, A., Di Giovanni, S., Hathout, Y., Natale, J. and Hoffman, E.P. (2006) Functional recovery of glycine receptors in spastic murine model of startle disease. Neurobiol. Dis., 21, 291-304.