Restricted ketogenic diet enhances the therapeutic action of N-butyldeoxynojirimycin towards brain GM2 accumulation in adult Sandhoff disease mice

Journal of Neurochemistry

Volumn 113, Issue 6, 2010, Pages 1525-1535

  Denny, Christine A ^a   Heinecke, Karie A ^a   Kim, Youngho P ^a   Baek, Rena C ^a   Loh, Katrina S ^a   Butters, Terry D ^b   Bronson, Roderick T ^c   Platt, Frances M ^d   Seyfried, Thomas N ^a  

^a BOSTON COLLEGE   (United States)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c DANA FARBER CANCER INSTITUTE   (United States)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

GA2; Ganglioside; GM2; Ketogenic diet; Lysosomal storage disease; Sandhoff disease

Indexed keywords

BETA N ACETYLHEXOSAMINIDASE; GANGLIOSIDE GM2; GLUCOSYLTRANSFERASE; GLYCOSPHINGOLIPID; MIGLUSTAT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CLINICAL EFFECTIVENESS; CONTROLLED STUDY; DIET RESTRICTION; FOREBRAIN; KETOGENIC DIET; KNOCKOUT MOUSE; LIPID STORAGE; LONGEVITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SANDHOFF DISEASE; THERAPY EFFECT; TREATMENT OUTCOME;

1-DEOXYNOJIRIMYCIN; 3-HYDROXYBUTYRIC ACID; ANALYSIS OF VARIANCE; ANIMALS; BETA-N-ACETYLHEXOSAMINIDASES; BLOOD GLUCOSE; BODY WEIGHT; BRAIN; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CHROMATOGRAPHY, THIN LAYER; EATING; G(M2) GANGLIOSIDE; KETOGENIC DIET; LIPID METABOLISM; MICE; MICE, KNOCKOUT; MYELIN SHEATH; PURKINJE CELLS; SANDHOFF DISEASE;

MURINAE; MUS;

EID: 77953105528     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.06733.x     Document Type: Article

References (50)

1. Alonzi D. S., Neville D. C. A., Lachmann R. H., Dwek R. A. Butters T. D. (2008) Glucosylated free oligosaccharides are biomarkers of endoplasmic- reticulum alpha-glucosidase inhibition. Biochem. J. 409, 571 580.
2. Andersson U., Butters T. D., Dwek R. A. Platt F. M. (2000) N-butyldeoxygalactonojirimycin: a more selective inhibitor of glycosphingolipid biosynthesis than N-butyldeoxynojirimycin, in vitro and in vivo. Biochem. Pharmacol. 59, 821 829.
3. Andersson U., Reinkensmeier G., Butters T., Dwek R. A. Platt F. M. (2004) Inhibition of glycogen breakdown by imino sugars in vitro and in vivo. Biochem. Pharmacol. 67, 697 705.
4. Ando S., Chang N. C. Yu R. K. (1978) High-performance thin-layer chromatography and densitometric determination of brain ganglioside compositions of several species. Anal. Biochem. 89, 437 450.
5. Arfi A., Bourgoin C., Basso L. et al. (2005) Bicistronic lentiviral vector corrects beta-hexosaminidase deficiency in transduced and cross-corrected human Sandhoff fibroblasts. Neurobiol. Dis. 20, 583 593.
6. Bae J. S. Kim B. J. (2005) Cerebellar ataxia and acute motor axonal neuropathy associated with Anti GD1b and Anti GM1 antibodies. J. Clin. Neurosci. 12, 808 810.
7. Baek R. C., Lee J. P., Seyfried T. N. Snyder E. Y. (2005) Neural stem cell transplantation reduces brain GM2 and GA2 content in a mouse model of Sandhoff disease. J. Neurochem. 94, 21.
8. Baek R. C., Kasperzyk J. L., Platt F. M. Seyfried T. N. (2008) N-butyldeoxygalactonojirimycin reduces brain ganglioside and GM2 content in neonatal Sandhoff disease mice. Neurochem. Int. 52, 1125 1133.
9. Begley D., Pontikis C. Scarpa M. (2008) Lysosomal storage diseases and the blood-brain barrier. Curr. Pharm. Des. 14, 1566 1580. (Pubitemid 352002984)
10. Cox T., Lachmann R., Hollak C. et al. (2000) Novel oral treatment of Gaucher's disease with N-butyldeoxynojirimycin (OGT 918) to decrease substrate biosynthesis. Lancet 355, 1481 1485.
11. Denny C. A., Kasperzyk J. L., Gorham K. N., Bronson R. T. Seyfried T. N. (2006) Influence of caloric restriction on motor behavior, longevity, and brain lipid composition in Sandhoff disease mice. J. Neurosci. Res. 83, 1028 1038.
12. Duan W., Guo Z., Jiang H., Ware M., Li X. J. Mattson M. P. (2003) Dietary restriction normalizes glucose metabolism and BDNF levels, slows disease progression, and increases survival in huntingtin mutant mice. Proc. Natl Acad. Sci. USA 100, 2911 2916.
13. Elstein D., Hollak C., Aerts J. M. F. G. et al. (2004) Sustained therapeutic effects of oral miglustat (Zavesca, N-butyldeoxynojirimycin, OGT 918) in type I Gaucher disease. J. Inherit. Metab. Dis. 27, 757 766.
14. Galjaard H. (1980) Genetic Metabolic Disease: Diagnosis and Prenatal Analysis. Elsevier Sicence Publishers
15. Giraldo P., Latre P., Alfonso P. et al. (2006) Short-term effect of miglustat in every day clinical use in treatment-naïve or previously treated patients with type 1 Gaucher's disease. Haematologica 91, 703 706.
16. Gjedde A. Crone C. (1975) Induction processes in blood-brain transfer of ketone bodies during starvation. Am. J. Physiol. 229, 1165 1169.
17. Gravel R. A., Clarke J. T. R., Kaback M. M., Mahuran D., Sandhoff K. Suzuki K. (1995) The GM2 gangliosidoses. in The Metabolic and Molecular Bases of Inherited Disease (Scriver C. R., Beaudet A. L., Sly W. S. Valle D., eds), Vol. II, pp. 2839 2879. McGraw-Hill, Inc.
18. Greene A. E., Todorova M. T., McGowan R. Seyfried T. N. (2001) Caloric restriction inhibits seizure susceptibility in epileptic EL mice by reducing blood glucose. Epilepsia 42, 1371 1378.
19. Hasselbalch S. G., Knudsen G. M., Jakobsen J., Hageman L. P., Holm S. Paulson O. B. (1995) Blood-brain barrier permeability of glucose and ketone bodies during short-term starvation in humans. Am. J. Physiol. 268, E1161 E1166.
20. Hauser E. C., Kasperzyk J. L., d'Azzo A. Seyfried T. N. (2004) Inheritance of lysosomal acid b-galactosidase activity and gangliosides in crosses of DBA/2J and knockout mice. Biochem. Genet. 42, 241 257.
21. Jeyakumar M., Butters T. D., Cortina-Borja M., Hunnam V., Proia R. L., Perry V. H., Dwek R. A. Platt F. M. (1999) Delayed symptom onset and increased life expectancy in Sandhoff disease mice treated with N-butyldeoxynojirimycin. Proc. Natl Acad. Sci. USA 96, 6388 6393.
22. Jeyakumar M., Norflus F., Tifft C. J., Cortina-Borja M., Butters T. D., Proia R. L., Perry V. H., Dwek R. A. Platt F. M. (2001) Enhanced survival in Sandhoff disease mice receiving a combination of substrate deprivation therapy and bone marrow transplantation. Blood 97, 327 329.
23. Kasperzyk J. L., El-Abbadi M. M., Hauser E. C., D'Azzo A., Platt F. M. Seyfried T. N. (2004) N-butyldeoxygalactonojirimycin reduces neonatal brain ganglioside content in a mouse model of GM1 gangliosidosis. J. Neurochem. 89, 645 653.
24. Kasperzyk J. L., d'Azzo A., Platt F. M., Alroy J. Seyfried T. N. (2005) Substrate reduction therapy reduces ganglioside content in postnatal cerebrum-brainstem and cerebellum in a mouse model of GM1 gangliosidosis. J. Lipid Res. 46, 744 751.
25. Lee C. K., Weindruch R. Prolla T. A. (2000) Gene-expression profile of the ageing brain in mice. Nat. Genet. 25, 294 297.
26. Macala L. J., Yu R. K. Ando S. (1983) Analysis of brain lipids by high performance thin-layer chromatography and densitometry. J. Lipid Res. 24, 1243 1250.
27. Mahoney L. B., Denny C. A. Seyfried T. N. (2006) Caloric restriction in C57BL/6J mice mimics therapeutic fasting in humans. Lipids Health Dis. 5, 13.
28. Mantis J. G., Centeno N., Todorova M. T., McGowan R. Seyfried T. N. (2003) Metabolic control of epilepsy in adult EL mice with the ketogenic diet and caloric restriction. Epilepsia 44 (Suppl. 9 64 65.
29. Mellor H. R., Adam A., Platt F. M., Dwek R. A. Butters T. D. (2000) High-performance cation-exchange chromatography and pulsed amperometric detection for the separation, detection, and quantitation of N-alkylated imino sugars in biological samples. Anal. Biochem. 284, 136 142.
30. Morgan T. E., Xie Z., Goldsmith S., Yoshida T., Lanzrein A.-S., Stone D., Rozovsky I., Perry G., Smith M. A. Finch C. E. (1999) The mosaic of brain glial hyperactivity during normal ageing and its attenuation by food restriction. Neuroscience 89, 687 699.
31. Mukherjee P., El-Abbadi M. M., Kasperzyk J. L., Ranes M. K. Seyfried T. N. (2002) Dietary restriction reduces angiogenesis and growth in an orthotopic mouse brain tumour model. Br. J. Cancer 86, 1615 1621.
32. Norflus F., Tifft C. J., McDonald M. P., Goldstein G., Crawley J. N., Hoffmann A., Sandhoff K., Suzuki K. Proia R. L. (1998) Bone marrow transplantation prolongs life span and ameliorates neurologic manifestations in Sandhoff disease mice. J. Clin. Invest. 101, 1881 1888.
33. Platt F. M., Neises G. R., Reinkensmeier G., Townsend M. J., Perry V. H., Proia R. L., Winchester B., Dwek R. A. Butters T. D. (1997) Prevention of lysosomal storage in Tay-Sachs mice treated with N- butyldeoxynojirimycin. Science 276, 428 431.
34. Platt F. M., Jeyakumar M., Andersson U., Heare T., Dwek R. A. Butters T. D. (2003) Substrate reduction therapy in mouse models of the glycosphingolipidoses. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358, 947 954.
35. Pollay M. Stevens F. A. (1980) Starvation-induced changes in transport of ketone bodies across the blood-brain barrier. J. Neurosci. Res. 5, 163 172.
36. Priestman D. A., van der Spoel A. C., Butters T. D., Dwek R. A. Platt F. M. (2008) N-butyldeoxynojirimycin causes weight loss as a result of appetite suppression in lean and obese mice. Diabetes Obes. Metab. 10, 159 166.
37. Pugh T. D., Klopp R. G. Weindruch R. (1999) Controlling caloric consumption: protocols for rodents and rhesus monkeys. Neurobiol. Aging 20, 157 165.
38. Ranes M. K., El-Abbadi M., Manfredi M. G., Mukherjee P., Platt F. M. Seyfried T. N. (2001) N -butyldeoxynojirimycin reduces growth and ganglioside content of experimental mouse brain tumours. Br. J. Cancer 84, 1107 1114.
39. Sandhoff K. Kolter T. (2003) Biosynthesis and degradation of mammalian glycosphingolipids. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358, 847 861.
40. Sango K., Yamanaka S., Hoffmann A. et al. (1995) Mouse models of Tay-Sachs and Sandhoff diseases differ in neurologic phenotype and ganglioside metabolism. Nat. Genet. 11, 170 176.
41. Seyfried T. N., Glaser G. H. Yu R. K. (1978) Cerebral, cerebellar, and brain stem gangliosides in mice susceptible to audiogenic seizures. J. Neurochem. 31, 21 27.
42. Seyfried T. N., Bernard D., Mayeda F., Macala L. Yu R. K. (1984) Genetic analysis of cerebellar lipids in mice susceptible to audiogenic seizures. Exp. Neurol. 84, 590 595.
43. Sugimoto H., Wakata N., Kishi M., Fujioka T., Kurihara T., Irie Y. Saito T. (2002) A case of Guillain-Barré syndrome associated with cerebellar ataxia and positive serum anti-GD1b IgG antibody. J. Neurol. 249, 346 347.
44. Tifft C. J. Proia R. L. (2000) Stemming the tide: glycosphingolipid synthesis inhibitors as therapy for storage diseases. Glycobiology 10, 1249 1258.
45. Todorova M. T., Tandon P., Madore R. A., Stafstrom C. E. Seyfried T. N. (2000) The ketogenic diet inhibits epileptogenesis in EL mice: a genetic model for idiopathic epilepsy. Epilepsia 41, 933 940.
46. Treiber A., Morand O. Clozel M. (2007) The pharmacokinetics and tissue distribution of the glucosylceramide synthase inhibitor. Xenobiotica 37, 298 314.
47. Veech R. L. (2004) The therapeutic implications of ketone bodies: the effects of ketone bodies in pathological conditions: ketosis, ketogenic diet, redox states, insulin resistance, and mitochondrial metabolism. Prostaglandins Leukot. Essent. Fatty Acids 70, 309 319.
48. Weindruch R. Walford R. L. (1988) The retardation of aging and disease by dietary restriction. Thomas
49. Willenbrock F. W., Neville D. C., Jacob G. S. Scudder P. (1991) The use of HPLC-pulsed amperometry for the characterization and assay of glycosidases and glycosyltransferases. Glycobiology 1, 223 227.
50. Williamson D. H., Mellanby J. Krebs H. A. (1962) Enzymic determination of D(-)-beta-hydroxybutyric acid and acetoacetic acid in blood. Biochem. J. 82, 90 96.