Pharmacological chaperones and coenzyme Q10 treatment improves mutant β-glucocerebrosidase activity and mitochondrial function in neuronopathic forms of gaucher disease

Scientific Reports

Volumn 5, Issue , 2015, Pages

  De La Mata, Mario ^a   Cotán, David ^a   Oropesa Ávila, Manuel ^a   Garrido Maraver, Juan ^a   Cordero, Mario D ^b   Paz, Marina Villanueva ^a   Pavón, Ana Delgado ^a   Alcocer Gómez, Elizabet ^a   De Lavera, Isabel ^a   Ybot González, Patricia ^c   Zaderenko, Ana Paula ^d   Mellet, Carmen Ortiz ^b   Fernández, José M García ^e   Sánchez Alcázar, José A ^a  

^a INSTITUTO DE SALUD CARLOS III   (Spain)

^b UNIVERSITY OF SEVILLE   (Spain)

^c HOSPITAL UNIVERSITARIO VIRGEN DEL ROCÍO   (Spain)

^d UNIVERSIDAD PABLO DE OLAVIDE   (Spain)

^e INSTITUTO DE INVESTIGACIONES QUÍMICAS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; ENZYME INHIBITOR; GLUCOSYLCERAMIDASE; REACTIVE OXYGEN METABOLITE; UBIDECARENONE; UBIQUINONE;

ANALOGS AND DERIVATIVES; AUTOPHAGY; DRUG EFFECTS; ENZYME ACTIVATION; FIBROBLAST; GAUCHER DISEASE; GENE EXPRESSION; GENETICS; HUMAN; METABOLISM; MITOCHONDRION; MUTATION; PHAGOSOME;

AUTOPHAGY; BIOMARKERS; ENZYME ACTIVATION; ENZYME INHIBITORS; FIBROBLASTS; GAUCHER DISEASE; GENE EXPRESSION; GLUCOSYLCERAMIDASE; HUMANS; MITOCHONDRIA; MUTATION; PHAGOSOMES; REACTIVE OXYGEN SPECIES; UBIQUINONE;

EID: 84930685986     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep10903     Document Type: Article

References (50)

1. Platt, F. M., Boland, B. & van der Spoel, A. C. The cell biology of disease: lysosomal storage disorders: the cellular impact of lysosomal dysfunction. J Cell Biol 199, 723-734 (2012).
2. Grabowski, G. A. Gaucher disease: gene frequencies and genotype/phenotype correlations. Genet Test 1, 5-12 (1997).
3. Barton, B., Zauber, S. E. & Goetz, C. G. Movement disorders caused by medical disease. Semin Neurol 29, 97-110 (2009).
4. Nalls, M. A. et al. A multicenter study of glucocerebrosidase mutations in dementia with Lewy bodies. JAMA Neurol 70, 727-735 (2013).
5. Sidransky, E. et al. Multicenter analysis of glucocerebrosidase mutations in Parkinson's disease. N Engl J Med 361, 1651-1661 (2009).
6. Westbroek, W., Gustafson, A. M. & Sidransky, E. Exploring the link between glucocerebrosidase mutations and parkinsonism. Trends Mol Med 17, 485-493 (2011).
7. de Pablo-Latorre, R. et al. Impaired parkin-mediated mitochondrial targeting to autophagosomes differentially contributes to tissue pathology in lysosomal storage diseases. Hum Mol Genet 21, 1770-1781 (2012).
8. Lebowitz, J. H. A breach in the blood-brain barrier. Proc Natl Acad Sci U S A 102, 14485-14486 (2005).
9. Schiffmann, R. et al. Randomized, controlled trial of miglustat in Gaucher's disease type 3. Ann Neurol 64, 514-522 (2008).
10. Zimran, A. & Elstein, D. Gaucher disease and the clinical experience with substrate reduction therapy. Philos Trans R Soc Lond B Biol Sci 358, 961-966 (2003).
11. Benito, J. M., Garcia Fernandez, J. M. & Ortiz Mellet, C. Pharmacological chaperone therapy for Gaucher disease: a patent review. Expert Opin Ther Pat 21, 885-903 (2011).
12. Sawkar, A. R., D'Haeze, W. & Kelly, J. W. Therapeutic strategies to ameliorate lysosomal storage disorders - a focus on Gaucher disease. Cell Mol Life Sci 63, 1179-1192 (2006).
13. Yoshida, H. ER stress and diseases. FEBS J 274, 630-658 (2007).
14. Tsuji, S. et al. A mutation in the human glucocerebrosidase gene in neuronopathic Gaucher's disease. N Engl J Med 316, 570-575 (1987).
15. Bendikov-Bar, I., Maor, G., Filocamo, M. & Horowitz, M. Ambroxol as a pharmacological chaperone for mutant glucocerebrosidase. Blood Cells Mol Dis 50, 141-145 (2013).
16. Compain, P. et al. Design and synthesis of highly potent and selective pharmacological chaperones for the treatment of Gaucher's disease. Chembiochem 7, 1356-1359 (2006).
17. Trapero, A., Gonzalez-Bulnes, P., Butters, T. D. & Llebaria, A. Potent aminocyclitol glucocerebrosidase inhibitors are subnanomolar pharmacological chaperones for treating gaucher disease. J Med Chem 55, 4479-4488 (2012).
18. Aguilar, M. et al. Molecular basis for β-glucosidase inhibition by ring-modified calystegine analogues. Chembiochem 9, 2612-2618 (2008).
19. Garcia-Moreno, M. I., Benito, J. M., Ortiz Mellet, C. & Garcia Fernandez, J. M. Synthesis and evaluation of calystegine B2 analogues as glycosidase inhibitors. J Org Chem 66, 7604-7614 (2001).
20. Alfonso, P. et al. Bicyclic derivatives of L-idonojirimycin as pharmacological chaperones for neuronopathic forms of Gaucher disease. Chembiochem 14, 943-949 (2013).
21. Aguilar-Moncayo, M. et al. Tuning glycosidase inhibition through aglycone interactions: pharmacological chaperones for Fabry disease and GM1 gangliosidosis. Chem Commun (Camb) 48, 6514-6516 (2011).
22. Rodriguez-Lavado, J. et al. Targeted delivery of pharmacological chaperones for Gaucher disease to macrophages by a mannosylated cyclodextrin carrier. Org Biomol Chem 12, 2289-2301 (2014).
23. Garcia Fernandez, J. M., Ortiz Mellet, C., Benito Hernandez, J. M. & Fuentes Mota, J. Synthesis of calystegine B2 analogs by tandem tautomerization-intramolecular glycosylation of thioureidosugars. Synlett 3 316-318 (1998).
24. Ebadi, M. et al. Ubiquinone (coenzyme Q10) and mitochondria in oxidative stress of parkinson's disease. Biol Signals Recept 10, 224-253 (2001).
25. Matalonga, L. et al. Treatment effect of coenzyme Q and an antioxidant cocktail in fibroblasts of patients with Sanfilippo disease. J Inherit Metab Dis 37, 439-446 (2014).
26. Haas, R.H. et al. The in-depth evaluation of suspected mitochondrial disease. Mol Genet Metab 94, 16-37 (2008).
27. Vander Heiden, M. G., Chandel, N. S., Williamson, E. K., Schumacker, P. T. & Thompson, C. B. Bcl-xL regulates the membrane potential and volume homeostasis of mitochondria. Cell 91, 627-637 (1997).
28. Scherz-Shouval, R. & Elazar, Z. Regulation of autophagy by ROS: physiology and pathology. Trends Biochem Sci 36, 30-38 (2011).
29. Garrido-Maraver, J. et al. Clinical applications of coenzyme Q10. Front Biosci (Landmark Ed) 19, 619-633 (2014).
30. Lieberman, A. P. et al. Autophagy in lysosomal storage disorders. Autophagy 8, 719-730 (2012).
31. Kim, I., Rodriguez-Enriquez, S. & Lemasters, J. J. Selective degradation of mitochondria by mitophagy. Arch Biochem Biophys 462, 245-253 (2007).
32. Schroder, B. A., Wrocklage, C., Hasilik, A. & Saftig, P. The proteome of lysosomes. Proteomics 10, 4053-4076 (2010).
33. Ezaki, J., Wolfe, L. S. & Kominami, E. Specific delay in the degradation of mitochondrial ATP synthase subunit c in late infantile neuronal ceroid lipofuscinosis is derived from cellular proteolytic dysfunction rather than structural alteration of subunit c. J Neurochem 67, 1677-1687 (1996).
34. Green, D. R., Galluzzi, L. & Kroemer, G. Mitochondria and the autophagy-inflammation-cell death axis in organismal aging. Science 333, 1109-1112 (2011).
35. Farfel-Becker, T. et al. Neuronal accumulation of glucosylceramide in a mouse model of neuronopathic Gaucher disease leads to neurodegeneration. Hum Mol Genet 23, 843-854 (2014).
36. Strasberg, P. Cerebrosides and psychosine disrupt mitochondrial functions. Biochem Cell Biol 64, 485-489 (1986).
37. Osellame, L. D. et al. Mitochondria and quality control defects in a mouse model of Gaucher disease-links to Parkinson's disease. Cell Metab 17, 941-953 (2013).
38. Sentelle, R. D. et al. Ceramide targets autophagosomes to mitochondria and induces lethal mitophagy. Nat Chem Biol 8, 831-838 (2012).
39. Fuller, M. et al. Glucosylceramide accumulation is not confined to the lysosome in fibroblasts from patients with Gaucher disease. Mol Genet Metab 93, 437-443 (2008).
40. Mitsui, J. et al. Mutations for Gaucher disease confer high susceptibility to Parkinson disease. Arch Neurol 66, 571-576 (2009).
41. Parenti, G. Treating lysosomal storage diseases with pharmacological chaperones: from concept to clinics. EMBO Mol Med 1, 268-279 (2009).
42. Boyd, R. E. et al. Pharmacological chaperones as therapeutics for lysosomal storage diseases. J Med Chem 56, 2705-2725 (2013).
43. Artuch, R. et al. Cerebrospinal fluid concentrations of idebenone in Friedreich ataxia patients. Neuropediatrics 35, 95-98 (2004).
44. Mizushima, N. et al. Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J Cell Biol 152, 657-668 (2001).
45. Aguilar-Moncayo, M. et al. Bicyclic (galacto)nojirimycin analogues as glycosidase inhibitors: effect of structural modifications in their pharmacological chaperone potential towards β-glucocerebrosidase. Org Biomol Chem 9, 3698-3713 (2011).
46. Rustin, P. et al. Biochemical and molecular investigations in respiratory chain deficiencies. Clin Chim Acta 228, 35-51 (1994).
47. Lowry, O. H., Rosebrough, N. J., Farr, A. L. & Randall, R. J. Protein measurement with the Folin phenol reagent. J Biol Chem 193, 265-275 (1951).
48. Rodriguez-Hernandez, A. et al. Coenzyme Q deficiency triggers mitochondria degradation by mitophagy. Autophagy 5, 19-32 (2009).
49. Cotan, D. et al. Secondary coenzyme Q10 deficiency triggers mitochondria degradation by mitophagy in MELAS fibroblasts. FASEB J 25, 2669-2687 (2011).
50. Brade, L., Vielhaber, G., Heinz, E. & Brade, H. In vitro characterization of anti-glucosylceramide rabbit antisera. Glycobiology 10, 629-636 (2000).