Identification of Niemann-Pick C1 disease biomarkers through sphingolipid profiling

Journal of Lipid Research

Volumn 54, Issue 10, 2013, Pages 2800-2814

  Fan, Martin ^a   Sidhu, Rohini ^a   Fujiwara, Hideji ^a   Tortelli, Brett ^a   Zhang, Jessie ^a   Davidson, Cristin ^b   Walkley, Steven U ^b   Bagel, Jessica H ^c   Vite, Charles ^c   Yanjanin, Nicole M ^d   Porter, Forbes D ^d   Schaffer, Jean E ^a   Ory, Daniel S ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

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

Author keywords

Metabolomics; Neurodegeneration; Sphingolipids

Indexed keywords

2 HYDROXYPROPYL BETA CYCLODEXTRIN; BIOLOGICAL MARKER; CERAMIDE; GANGLIOSIDE GM2; GANGLIOSIDE GM3; MIGLUSTAT; MONOHEXOSYLCERAMIDE; SPHINGOLIPID; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BAGG ALBINO MOUSE; BIOACCUMULATION; CEREBROSPINAL FLUID LEVEL; CONTROLLED STUDY; DRUG RESPONSE; HUMAN; LIPID ANALYSIS; LIPID BLOOD LEVEL; MASS SPECTROMETRY; MOUSE; NIEMANN PICK DISEASE; NONHUMAN; PRIORITY JOURNAL;

METABOLOMICS; NEURODEGENERATION; SPHINGOLIPIDS;

1-DEOXYNOJIRIMYCIN; ANIMALS; BETA-CYCLODEXTRINS; BIOLOGICAL MARKERS; CATS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DRUG EVALUATION, PRECLINICAL; FEMALE; GANGLIOSIDES; HUMANS; MALE; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; NIEMANN-PICK DISEASE, TYPE C; ORGAN SPECIFICITY; SPHINGOLIPIDS; SULFOGLYCOSPHINGOLIPIDS; TANDEM MASS SPECTROMETRY;

EID: 84884164889     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M040618     Document Type: Article

References (50)

1. Vanier, M. T. 2010. Niemann-Pick disease type C. Orphanet J. Rare Dis. 5: 16.
2. Carstea, E. D., J. A. Morris, K. G. Coleman, S. K. Loftus, D. Zhang, C. Cummings, J. Gu, M. A. Rosenfeld, W. J. Pavan, D. B. Krizman, et al. 1997. Niemann-Pick C1 disease gene: homology to mediators of cholesterol homeostasis. Science. 277: 228-231.
3. Vanier, M. T., S. Duthel, C. Rodriguez-Lafrasse, P. Pentchev, and E. D. Carstea. 1996. Genetic heterogeneity in Niemann-Pick C disease: a study using somatic cell hybridization and linkage analysis. Am. J. Hum. Genet. 58: 118-125.
4. Naureckiene, S., D. E. Sleat, H. Lackland, A. Fensom, M. T. Vanier, R. Wattiaux, M. Jadot, and P. Lobel. 2000. Identification of HE1 as the second gene of Niemann-Pick C disease. Science. 290: 2298-2301.
5. Vanier, M. T., and G. Millat. 2003. Niemann-Pick disease type C. Clin. Genet. 64: 269-281.
6. Vanier, M. T. 1983. Biochemical studies in Niemann-Pick disease. I. Major sphingolipids of liver and spleen. Biochim. Biophys. Acta. 750: 178-184.
7. Vanier, M. T. 1999. Lipid changes in Niemann-Pick disease type C brain: personal experience and review of the literature. Neurochem. Res. 24: 481-489.
8. Tint, G. S., P. Pentchev, G. Xu, A. K. Batta, S. Shiefer, G. Salen, and A. Honda. 1998. Cholesterol and oxygenated cholesterol concentrations are markedly elevated in peripheral tissue but not in brain from mice with Niemann-Pick type C phenotype. J. Inherit. Metab. Dis. 21: 853-863.
9. Zhang, J. R., T. Coleman, S. J. Langmade, D. E. Scherrer, L. Lane, M. H. Lanier, C. Feng, M. S. Sands, J. E. Schaffer, C. F. Semenkovich, et al. 2008. Niemann-Pick C1 protects against atherosclerosis in mice via regulation of macrophage intracellular cholesterol trafficking. J. Clin. Invest. 118: 2281-2290.
10. Porter, F. D., D. E. Scherrer, M. H. Lanier, S. J. Langmade, V. Molugu, S. E. Gale, D. Olzeski, R. Sidhu, D. J. Dietzen, R. Fu, et al. 2010. Cholesterol oxidation products are sensitive and specific blood-based biomarkers for Niemann-Pick C1 disease. Sci. Transl. Med. 2: 56ra81.
11. Walkley, S. U., and K. Suzuki. 2004. Consequences of NPC1 and NPC2 loss of function in neurons. Biochim. Biophys. Acta. 1685: 48-62.
12. Sarna, J. R., M. Larouche, H. Marzban, R. V. Sillitoe, D. E. Rancourt, and R. Hawkes. 2003. Patterned Purkinje cell degeneration in mouse models of Niemann-Pick type C disease. J. Comp. Neurol. 456: 279-291.
13. Higashi, Y., S. Murayama, P. G. Pentchev, and K. Suzuki. 1993. Cerebellar degeneration in the Niemann-Pick type C mouse. Acta Neuropathol. 85: 175-184.
14. Loftus, S. K., J. A. Morris, E. D. Carstea, J. Z. Gu, C. Cummings, A. Brown, J. Ellison, K. Ohno, M. A. Rosenfeld, D. A. Tagle, et al. 1997. Murine model of Niemann-Pick C disease: mutation in a cholesterol homeostasis gene. Science. 277: 232-235.
15. Pentchev, P. G., A. E. Gal, A. D. Booth, F. Omodeo-Sale, J. Fouks, B. A. Neumeyer, J. M. Quirk, G. Dawson, and R. O. Brady. 1980. A lysosomal storage disorder in mice characterized by a dual deficiency of sphingomyelinase and glucocerebrosidase. Biochim. Biophys. Acta. 619: 669-679.
16. Reid, P. C., N. Sakahita, S. Sugii, Y. Ohno-Iwashita, Y. Shimada, W. F. Hickey, and T. Y. Chang. 2004. A novel cholesterol stain reveals early neuronal cholesterol accumulation in the Niemann-Pick type C1 mouse brain. J. Lipid Res. 45: 582-591.
17. Ko, D. C., L. Milenkovic, S. M. Beier, H. M. Anuel, J. Buchanan, and M. P. Scott. 2005. Cell-autonomous death of cerebellar Purkinje neurons with autophagy in Niemann-Pick type C disease. PLoS Genet. 1: 81-95.
18. Wu, Y-P., H. Mizukami, J. Matsuda, Y. Saito, R. Proia, and K. Suzuki. 2005. Apoptosis accompanied by up-regulation of TNF-alpha death pathway genes in the brain of Niemann-Pick type C disease. Mol. Genet. Metab. 84: 9-17.
19. Somers, K. L., M. A. Royals, E. D. Carstea, M. A. Rafi, D. A. Wenger, and M. A. Thrall. 2003. Mutation analysis of feline Niemann-Pick C1 disease. Mol. Genet. Metab. 79: 99-103.
20. Vite, C. H., W. Ding, C. Bryan, P. O'Donnell, K. Cullen, D. Aleman, M. E. Haskins, and T. Van Winkle. 2008. Clinical, electrophysiological, and serum biochemical measures of progressive neurological and hepatic dysfunction in feline Niemann-Pick type C disease. Pediatr. Res. 64: 544-549.
21. Davidson, C. D., N. F. Ali, M. C. Micsenyi, G. Stephney, S. Renault, K. Dobrenis, D. S. Ory, M. T. Vanier, and S. U. Walkley. 2009. Chronic cyclodextrin treatment of murine Niemann-Pick C disease ameliorates neuronal cholesterol and glycosphingolipid storage and disease progression. PLoS ONE. 4: e6951.
22. Liu, B., H. Li, J. J. Repa, S. D. Turley, and J. M. Dietschy. 2008. Genetic variations and treatments that affect the lifespan of the NPC1 mouse. J. Lipid Res. 49: 663-669.
23. Liu, B., C. M. Ramirez, A. M. Miller, J. J. Repa, S. D. Turley, and J. M. Dietschy. 2010. Cyclodextrin overcomes the transport defect in nearly every organ of NPC1 mice leading to excretion of sequestered cholesterol as bile acid. J. Lipid Res. 51: 933-944.
24. Liu, B., S. D. Turley, D. K. Burns, A. M. Miller, J. J. Repa, and J. M. Dietschy. 2009. Reversal of defective lysosomal transport in NPC disease ameliorates liver dysfunction and neurodegeneration in the npc1-/- mouse. Proc. Natl. Acad. Sci. USA. 106: 2377-2382.
25. Ward, S., P. O'Donnell, S. Fernandez, and C. H. Vite. 2010. 2-hydroxypropyl-beta-cyclodextrin raises hearing threshold in normal cats and in cats with Niemann-Pick type C disease. Pediatr. Res. 68: 52-56.
26. Stein, V. M., A. Crooks, W. Ding, M. Prociuk, P. O'Donnell, C. Bryan, T. Sikora, J. Dingemanse, M. T. Vanier, S. U. Walkley, et al. 2012. Miglustat improves purkinje cell survival and alters microglial phenotype in feline Niemann-Pick disease type C. J. Neuropathol. Exp. Neurol. 71: 434-448.
27. Matsuo, M., M. Togawa, K. Hirabaru, S. Mochinaga, A. Narita, M. Adachi, M. Egashira, T. Irie, and K. Ohno. 2013. Effects of cyclodextrin in two patients with Niemann-Pick type C disease. Mol. Genet. Metab. 108: 76-81.
28. Patterson, M. C., D. Vecchio, H. Prady, L. Abel, and J. E. Wraith. 2007. Miglustat for treatment of Niemann-Pick C disease: a randomised controlled study. Lancet Neurol. 6: 765-772.
29. Zervas, M., K. L. Somers, M. A. Thrall, and S. U. Walkley. 2001. Critical role for glycosphingolipids in Niemann-Pick disease type C. Curr. Biol. 11: 1283-1287.
30. Shaner, R. L., J. C. Allegood, H. Park, E. Wang, S. Kelly, C. A. Haynes, M. C. Sullards, and A. H. Merrill, Jr. 2009. Quantitative analysis of sphingolipids for lipidomics using triple quadrupole and quadrupole linear ion trap mass spectrometers. J. Lipid Res. 50: 1692-1707.
31. Ikeda, K., T. Shimizu, and R. Taguchi. 2008. Targeted analysis of ganglioside and sulfatide molecular species by LC/ESI-MS/MS with theoretically expanded multiple reaction monitoring. J. Lipid Res. 49: 2678-2689.
32. Goldin, E., C. F. Roff, S. P. Miller, C. Rodriguez-Lafrasse, M. T. Vanier, R. O. Brady, and P. G. Pentchev. 1992. Type C Niemann- Pick disease: a murine model of the lysosomal cholesterol lipidosis accumulates sphingosine and sphinganine in liver. Biochim. Biophys. Acta. 1127: 303-311.
33. Pentchev, P. G., A. D. Boothe, H. S. Kruth, H. Weintroub, J. Stivers, and R. O. Brady. 1984. A genetic storage disorder in BALB/C mice with a metabolic block in esterification of exogenous cholesterol. J. Biol. Chem. 259: 5784-5791.
34. Sleat, D. E., J. A. Wiseman, M. El-Banna, S. M. Price, L. Verot, M. M. Shen, G. S. Tint, M. T. Vanier, S. U. Walkley, and P. Lobel. 2004. Genetic evidence for nonredundant functional cooperativity between NPC1 and NPC2 in lipid transport. Proc. Natl. Acad. Sci. USA. 101: 5886-5891.
35. Quehenberger, O., A. M. Armando, A. H. Brown, S. B. Milne, D. S. Myers, A. H. Merrill, S. Bandyopadhyay, K. N. Jones, S. Kelly, R. L. Shaner, et al. 2010. Lipidomics reveals a remarkable diversity of lipids in human plasma. J. Lipid Res. 51: 3299-3305.
36. Zhou, S., C. Davidson, R. McGlynn, G. Stephney, K. Dobrenis, M. T. Vanier, and S. U. Walkley. 2011. Endosomal/lysosomal processing of gangliosides affects neuronal cholesterol sequestration in Niemann-Pick disease type C. Am. J. Pathol. 179: 890-902.
37. Pentchev, P. G., M. Vanier, K. Suzuki, and M. Patterson. 1995. Niemann-Pick disease type C: a lipid trafficking disorder. In The Metabolic and Molecular Basis of Inherited Diseases. C. Scriver, A. Beaudet, W. Sly, and D. Valle, editors. McGraw-Hill, Philadelphia, PA. 2625-2639.
38. Dacremont, G., J. A. Kint, D. Carton, and G. Cocquyt. 1974. Glucosylceramide in plasma of patients with Niemann-Pick disease. Clin. Chim. Acta. 52: 365-367.
39. Devlin, C., N. H. Pipalia, X. Liao, E. H. Schuchman, F. R. Maxfield, and I. Tabas. 2010. Improvement in lipid and protein trafficking in Niemann-Pick C1 cells by correction of a secondary enzyme defect. Traffic. 11: 601-615.
40. Reagan, J. W., Jr ., M. L. Hubbert, and G. S. Shelness. 2000. Posttranslational regulation of acid sphingomyelinase in Niemann- Pick type C1 fibroblasts and free cholesterol-enriched chinese hamster ovary cells. J. Biol. Chem. 275: 38104-38110.
41. Merrill, A. H., Jr ., S. Lingrell, E. Wang, M. Nikolova-Karakashian, T. R. Vales, and D. E. Vance. 1995. Sphingolipid biosynthesis de novo by rat hepatocytes in culture. Ceramide and sphingomyelin are associated with, but not required for, very low density lipoprotein secretion. J. Biol. Chem. 270: 13834-13841.
42. Memon, R. A., W. M. Holleran, A. H. Moser, T. Seki, Y. Uchida, J. Fuller, J. K. Shigenaga, C. Grunfeld, and K. R. Feingold. 1998. Endotoxin and cytokines increase hepatic sphingolipid biosynthesis and produce lipoproteins enriched in ceramides and sphingomyelin. Arterioscler. Thromb. Vasc. Biol. 18: 1257-1265.
43. de Gassart, A., C. Geminard, B. Fevrier, G. Raposo, and M. Vidal. 2003. Lipid raft-associated protein sorting in exosomes. Blood. 102: 4336-4344.
44. Strauss, K., C. Goebel, H. Runz, W. Moebius, S. Weiss, I. Feussner, M. Simons, and A. Schneider. 2010. Exosome secretion ameliorates lysosomal storage of cholesterol in Niemann-Pick type C disease. J. Biol. Chem. 285: 26279-26288.
45. Ashe, K. M., D. Bangari, L. Li, M. A. Cabrera-Salazar, S. D. Bercury, J. B. Nietupski, C. G. Cooper, J. M. Aerts, E. R. Lee, D. P. Copeland, et al. 2011. Iminosugar-based inhibitors of glucosylceramide synthase increase brain glycosphingolipids and survival in a mouse model of Sandhoff disease. PLoS ONE. 6: e21758.
46. Nietupski, J. B., J. J. Pacheco, W. L. Chuang, K. Maratea, L. Li, J. Foley, K. M. Ashe, C. G. Cooper, J. M. Aerts, D. P. Copeland, et al. 2012. Iminosugar-based inhibitors of glucosylceramide synthase prolong survival but paradoxically increase brain glucosylceramide levels in Niemann-Pick C mice. Mol. Genet. Metab. 105: 621-628.
47. Walden, C. M., R. Sandhoff, C. C. Chuang, Y. Yildiz, T. D. Butters, R. A. Dwek, F. M. Platt, and A. C. van der Spoel. 2007. Accumulation of glucosylceramide in murine testis, caused by inhibition of betaglucosidase 2: implications for spermatogenesis. J. Biol. Chem. 282: 32655-32664.
48. Chen, F. W., C. Li, and Y. A. Ioannou. 2010. Cyclodextrin induces calcium-dependent lysosomal exocytosis. PLoS ONE. 5: e15054.
49. Jiang, X., R. Sidhu, F. D. Porter, N. M. Yanjanin, A. O. Speak, D. T. te Vruchte, F. M. Platt, H. Fujiwara, D. E. Scherrer, J. Zhang, et al. 2011. A sensitive and specific LC-MS/MS method for rapid diagnosis of Niemann-Pick C1 disease from human plasma. J. Lipid Res. 52: 1435-1445.
50. Cluzeau, C. V., D. E. Watkins-Chow, R. Fu, B. Borate, N. Yanjanin, M. K. Dail, C. D. Davidson, S. U. Walkley, D. S. Ory, C. A. Wassif, et al. 2012. Microarray expression analysis and identification of serum biomarkers for Niemann-Pick disease, type C1. Hum. Mol. Genet. 21: 3632-3646.