Oxidative stress in Niemann-Pick type C patients: A protective role of N-butyl-deoxynojirimycin therapy

International Journal of Developmental Neuroscience

Volumn 30, Issue 6, 2012, Pages 439-444

  Ribas, Graziela S ^a,b   Pires, Ricardo ^c   Coelho, Janice Carneiro ^a   Rodrigues, Daiane ^b   Mescka, Caroline Paula ^a,b   Vanzin, Camila S ^a,b   Biancini, Giovana B ^a,b   Negretto, Giovanna ^a,b   Wayhs, Carlos A Y ^a,b   Wajner, Moacir ^a,b   Vargas, Carmen R ^a,b  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^b HOSPITAL DE CLÍNICAS DE PORTO ALEGRE   (Brazil)

^c UNIVERSIDADE LUTERANA DO BRASIL   (Brazil)

Author keywords

Antioxidants; Lysosomal storage disorder; N butyl deoxynojirimycin; Niemann Pick type C; Oxidative stress

Indexed keywords

BIOLOGICAL MARKER; CATALASE; GLUTATHIONE PEROXIDASE; MIGLUSTAT; SUPEROXIDE DISMUTASE; THIOBARBITURIC ACID REACTIVE SUBSTANCE;

ADOLESCENT; ADULT; ANTIOXIDANT ACTIVITY; ARTICLE; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ASSAY; ERYTHROCYTE; FIBROBLAST; HUMAN; HUMAN CELL; IN VIVO STUDY; INFANT; LIPID OXIDATION; NEUROPROTECTION; NIEMANN PICK DISEASE; OXIDATIVE STRESS; PLASMA; PRESCHOOL CHILD; PRIORITY JOURNAL; PROTEIN CARBONYLATION; PROTEIN DETERMINATION; SCHOOL CHILD; TOTAL ANTIOXIDANT STATUS;

1-DEOXYNOJIRIMYCIN; ADOLESCENT; ADULT; ANTIOXIDANTS; CATALASE; CHILD; ENZYME INHIBITORS; ERYTHROCYTES; FEMALE; FIBROBLASTS; GLUTATHIONE; GLUTATHIONE PEROXIDASE; HUMANS; INFANT; LONGITUDINAL STUDIES; MALE; NIEMANN-PICK DISEASE, TYPE C; OXIDATIVE STRESS; PLASMA; PROTEIN CARBONYLATION; STATISTICS, NONPARAMETRIC; SUPEROXIDE DISMUTASE; THIOBARBITURIC ACID REACTIVE SUBSTANCES; YOUNG ADULT;

EID: 84865865703     PISSN: 07365748     EISSN: 1873474X     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2012.07.002     Document Type: Article

References (56)

1. Aebi H. Catalase in vitro. Methods in Enzymology 1984, 105:121-126.
2. Baudry M., Yao Y., Simmons D., Liu J., Bi X. Postnatal development of inflammation in a murine model of Niemann-Pick type C disease: immunohistochemical observations of microglia and astroglia. Experimental Neurology 2003, 184:887-903.
3. Bhatti G.K., Bhatti J.S., Kiran R., Sandhir R. Alterations in Ca(2+) homeostasis and oxidative damage induced by ethion in erythrocytes of Wistar rats: ameliorative effect of vitamin E. Environmental Toxicology and Pharmacology 2011, 31:378-386.
4. Browne R.W., Armstrong D. Reduced glutathione and glutathione disulfide. Methods in Molecular Biology 1998, 108:347-352.
5. Cenedella R.J. Cholesterol synthesis inhibitor U18666A and the role of sterol metabolism and trafficking in numerous pathophysiological processes. Lipids 2009, 44:477-487.
6. Coelho J.A., Giugliani R. Fibroblasts of skin fragments as a tool for the investigation of genetic diseases: technical recommendations. Genetics and Molecular Biology 2000, 23:269-271.
7. Colomé C., Artuch R., Vilaseca M.A., Sierra C., Brandi N., Lambruschini N., Cambra F.J., Campistol J. Lipophilic antioxidants in patients with phenylketonuria. American Journal of Clinical Nutrition 2003, 77:185-188.
8. Dalle-Donne I., Rossi R., Giustarini D., Milzani A., Colombo R. Protein carbonyl groups as biomarkers of oxidative stress. Clinica Chimica Acta 2003, 329:23-38.
9. Dalle-Donne I., Aldini G., Carini M., Colombo R., Rossi R., Milzani A. Protein carbonylation, cellular dysfunction, and disease progression. Journal of Cellular and Molecular Medicine 2006, 10:389-406.
10. Deon M., Wajner M., Sirtori L.R., Fitarelli D., Coelho D.M., Sitta A., Barschak A.G., Ferreira G.C., Haeser A., Giugliani R., Vargas C.R. The effect of Lorenzo's oil on oxidative stress in X-linked adrenoleukodystrophy. Journal of the Neurological Sciences 2006, 247:157-164.
11. Evans P., Halliwell B. Free radicals and hearing: cause, consequence, and criteria. Annals of the New York Academy of Sciences 1999, 884:19-40.
12. Fernández A., Llacuna L., Fernández-Checa J.C., Colell A. Mitochondrial cholesterol loading exacerbates amyloid beta peptide-induced inflammation and neurotoxicity. Journal of Neuroscience 2009, 29:6394-6405.
13. Filippon L., Vanzin C.S., Biancini G.B., Pereira I.N., Manfredini V., Sitta A., Peralba Mdo C., Schwartz I.V., Giugliani R., Vargas C.R. Oxidative stress in patients with mucopolysaccharidosis type II before and during enzyme replacement therapy. Molecular Genetics and Metabolism 2011, 103:121-127.
14. Frolov A., Zielinski S.E., Crowley J.R., Dudley-Rucker N., Schaffer J.E., Ory D.S. NPC1 and NPC2 regulate cellular cholesterol homeostasis through generation of low density lipoprotein cholesterol-derived oxysterols. Journal of Biological Chemistry 2003, 278:25517-25525.
15. Fu R., Yanjanin N.M., Bianconi S., Pavan W.J., Porter F.D. Oxidative stress in Niemann-Pick disease, type C. Molecular Genetics and Metabolism 2010, 101:214-218.
16. Ghosh B., Hanevold C.D., Dobashi K., Orak J.K., Singh I. Tissue differences in antioxidant enzyme gene expression in response to endotoxin. Free Radical Biology and Medicine 1996, 21:533-540.
17. Griffin L.D., Gong W., Verot L., Mellon S.H. Niemann-Pick type C disease involves disrupted neurosteroidogenesis and responds to allopregnanolone. Nature Medicine 2004, 10:704-711.
18. Halliwell B., Gutteridge J.M.C. Free Radicals in Biology and Medicine 2007, Oxford University Press, New York.
19. Levine R.L., Garland D., Oliver C.N., Amici A., Climent L., Lenz A.G., Ahn B.W., Shalthiel S., Stadman E.R. Determination of carbonyl content in oxidatively modified proteins. Methods in Enzymology 1990, 186:464-478.
20. Liscum L., Ruggiero R.M., Faust J.R. The intracellular transport of low density lipoprotein-derived cholesterol is defective in Niemann-Pick type C fibroblasts. Journal of Cell Biology 1989, 108:1625-1636.
21. Lloyd-Evans E., Pelled D., Riebeling C., Bodennec J., de-Morgan A., Waller H., Schiffmann R., Futerman A.H. Glucosylceramide and glucosylsphingosine modulate calcium mobilization from brain microsomes via different mechanisms. Journal of Biological Chemistry 2003, 278:23594-23599.
22. Lloyd-Evans E., Morgan A.J., He X., Smith D.A., Elliot-Smith E., Sillence D.J., Churchill G.C., Schuchman E.H., Galione A., Platt F.M. Niemann-Pick disease type C1 is a sphingosine storage disease that causes deregulation of lysosomal calcium. Nature Medicine 2008, 14:1247-1255.
23. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry 1951, 193:265-275.
24. Madra M., Sturley S.L. Niemann-Pick type C pathogenesis and treatment: from statins to sugars. Clinical Lipidology 2010, 5:387-395.
25. Miller N.J., Rice-Evans C., Davies M.J., Gopinathan V., Milner A. A novel method for measuring antioxidant capacity and its application to monitoring the antioxidant status in premature neonates. Clinical Science 1993, 84:407-412.
26. Ohkawa H., Chishi N., Yagi K. Assay for lipid peroxides in animal tissue of thiobarbituric acid reaction. Analytical Biochemistry 1979, 95:351-358.
27. Pastores G.M., Barnett N.L. Substrate reduction therapy: miglustat as a remedy for symptomatic patients with Gaucher disease type 1. Expert Opinion on Investigational Drugs 2003, 12:273-281.
28. Patterson M.C., Vecchio D., Prady H., Abel L., Wraith J.E. Miglustat for treatment of Niemann-Pick C disease: a randomised controlled study. Lancet Neurology 2007, 6:765-772.
29. Paul C.A., Boegle A.K., Maue R.A. Before the loss: neuronal dysfunction in Niemann-Pick Type C disease. Biochimica et Biophysica Acta 2004, 1685:63-76.
30. Pentchev P.G., Vanier M.T., Suzuki K., Patterson M.C. Niemann Pick type C: a cellular cholesterol lipidosis. The Metabolic and Molecular Bases of Inherited Disease 2001, 2625-2639. Mc-GrawHill Inc, New York. 8th ed. C.R. Scriver, A.L. Beaudet, W.S. Sly, D. Valle (Eds.).
31. Pereira V.G., Martins A.M., Micheletti C., D'Almeida V. Mutational and oxidative stress analysis in patients with mucopolysaccharidosis type I undergoing enzyme replacement therapy. Clinica Chimica Acta 2007, 387:75-79.
32. Pineda M., Wraith J.E., Mengel E., Sedel F., Hwu W.L., Rohrbach M., Bembi B., Walterfang M., Korenke G.C., Marquardt T., Luzy C., Giorgino R., Patterson M.C. Miglustat in patients with Niemann-Pick disease Type C (NP-C): a multicenter observational retrospective cohort study. Molecular Genetics and Metabolism 2009, 98:243-249.
33. Porter F.D., Scherrer D.E., Lanier M.H., Langmade S.J., Molugu V., Gale S.E., Olzeski D., Sidhu R., Dietzen D.J., Fu R., Wassif C.A., Yanjanin N.M., Marso S.P., House J., Vite C., Schaffer J.E., Ory D.S. Cholesterol oxidation products are sensitive and specific blood-based biomarkers for Niemann-Pick C1 disease. Science Translational Medicine 2010, 2:56ra81.
34. Reddy J.V., Ganley I.G., Pfeffer S.R. Clues to neuro-degeneration in Niemann-Pick type C disease from global gene expression profiling. PLoS One 2006, 1:e19.
35. Reolon G.K., Reinke A., de Oliveira M.R., Braga L.M., Camassola M., Andrades M.E., Moreira J.C., Nardi N.B., Roesler R., Dal-Pizzol F. Alterations in oxidative markers in the cerebellum and peripheral organs in MPS I mice. Cellular and Molecular Neurobiology 2009, 29:443-448.
36. Ribas G.S., Sitta A., Wajner M., Vargas C.R. Oxidative stress in phenylketonuria: what is the evidence?. Cellular and Molecular Neurobiology 2011, 31:653-662.
37. Roversi F.M., Galdieri L.C., Grego B.H., Souza F.G., Micheletti C., Martins A.M., D'Almeida V. Blood oxidative stress markers in Gaucher disease patients. Clinica Chimica Acta 2006, 364:316-320.
38. Schedin S., Sindelar P.J., Pentchev P., Brunk U., Dallner G. Peroxisomal impairment in Niemann-Pick type C disease. Journal of Biological Chemistry 1997, 272:6245-6251.
39. Sturley S.L., Patterson M.C., Balch W., Liscum L. The pathophysiology and mechanisms of NP-C disease. Biochimica et Biophysica Acta 2004, 1685:83-87.
40. Suzuki H., Sakiyama T., Harada N., Abe M., Tadokoro M. Pathologic changes of glial cells in murine model of Niemann-Pick disease type C: immunohistochemical, lectin-histochemical and ultrastructural observations. Pediatrics International 2003, 45:1-4.
41. te Vruchte D., Lloyd-Evans E., Veldman R.J., Neville D.C., Dwek R.A., Platt F.M., van Blitterswijk W.J., Sillence D.J. Accumulation of glycosphingolipids in Niemann-Pick C disease disrupts endosomal transport. Journal of Biological Chemistry 2004, 279:26167-26175.
42. Terman A., Kurz T., Gustafsson B., Brunk U.T. Lysosomal labilization. IUBMB Life 2006, 58:531-539.
43. Tint G.S., Pentchev P., Xu G., Batta A.K., Shefer S., Salen G., Honda A. Cholesterol and oxygenated cholesterol concentrations are markedly elevated in peripheral tissue but not in brain from mice with the Niemann-Pick type C phenotype. Journal of Inherited Metabolic Disease 1998, 21:853-863.
44. van Giersbergen P.L., Dingemanse J. Influence of food intake on the pharmacokinetics of miglustat, an inhibitor of glucosylceramide synthase. Journal of Clinical Pharmacology 2007, 47:1277-1282.
45. Vanier M.T. Niemann-Pick disease type C. Orphanet Journal of Rare Diseases 2010, 5:16.
46. Vázquez M.C., Del Pozo T., Robledo F.A., Carrasco G., Pavez L., Olivares F., González M., Zanlungo S. Alteration of gene expression profile in Niemann-Pick type C mice correlates with tissue damage and oxidative stress. PLoS One 2011, 6:e28777.
47. Wajner M., Latini A., Wyse A.T., Dutra-Filho C.S. The role of oxidative damage in the neuropathology of organic acidurias: insights from animal studies. Journal of Inherited Metabolic Disease 2004, 27:427-448.
48. Walkley S.U., Suzuki K. Consequences of NPC1 and NPC2 loss of function in mammalian neurons. Biochimica et Biophysica Acta 2004, 1685:48-62.
49. Wendel A. Glutathione peroxidase. Methods in Enzymology 1981, 77:325-332.
50. Wraith J.E., Imrie J. New therapies in the management of Niemann-Pick type C disease: clinical utility of miglustat. Therapeutics and Clinical Risk Management 2009, 5:877-887.
51. Wraith J.E., Vecchio D., Jacklin E., Abel L., Chadha-Boreham H., Luzy C., Giorgino R., Patterson M.C. Miglustat in adult and juvenile patients with Niemann-Pick disease type C: long-term data from a clinical trial. Molecular Genetics and Metabolism 2010, 99:351-357.
52. Wu Y.P., Mizukami H., Matsuda J., Saito Y., Proia R.L., Suzuki K. Apoptosis accompanied by up-regulation of TNF-alpha death pathway genes in the brain of Niemann-Pick type C disease. Molecular Genetics and Metabolism 2005, 84:9-17.
53. Zampieri S., Mellon S.H., Butters T.D., Nevyjel M., Covey D.F., Bembi B., Dardis A. Oxidative stress in NPC1 deficient cells: protective effect of allopregnanolone. Journal of Cellular and Molecular Medicine 2009, 13:3786-3796.
54. Zarowski M., Steinborn B., Gurda B., Dvorakova L., Vlaskova H., Kothare S.V. Treatment of cataplexy in Niemann-Pick disease type C with the use of miglustat. European Journal of Paediatric Neurology 2011, 5:84-87.
55. Zervas M., Dobrenis K., Walkley S.U. Neurons in Niemann-Pick disease type C accumulate gangliosides as well as unesterified cholesterol and undergo dendritic and axonal alterations. Journal of Neuropathology and Experimental Neurology 2001, 60:49-64.
56. Zhang J.R., Coleman T., Langmade S.J., Scherrer D.E., Lane L., Lanier M.H., Feng C., Sands M.S., Schaffer J.E., Semenkovich C.F., Ory D.S. Niemann-Pick C1 protects against atherosclerosis in mice via regulation of macrophage intracellular cholesterol trafficking. Journal of Clinical Investigation 2008, 118:2281-2290.