Plasma signature of neurological disease in the monogenetic disorder Niemann-Pick type C

Journal of Biological Chemistry

Volumn 289, Issue 12, 2014, Pages 8051-8066

  Alam, Md Suhail ^a   Getz, Michelle ^a   Yi, Sue ^a   Kurkewich, Jeffrey ^a   Safeukui, Innocent ^a   Haldar, Kasturi ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD; CYCLODEXTRINS; ENZYMES; MAMMALS; NEUROLOGY; PATHOLOGY; PLASMAS;

EARLY DIAGNOSIS; INFLAMMATORY DISEASE; INTRAPERITONEALLY; MICROARRAY ANALYSIS; NEURODEGENERATION; NEUROLOGICAL DISEASE; NEUROLOGICAL DISORDERS; NIEMANN-PICK TYPE C;

DIAGNOSIS;

2 HYDROXYPROPYL BETA CYCLODEXTRIN; 24 HYDROXYCHOLESTEROL; BIOLOGICAL MARKER; CATHEPSIN B; CATHEPSIN D; CATHEPSIN S; CHOLESTEROL DERIVATIVE; LYSOZYME; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CEREBELLUM; CONTROLLED STUDY; DEGENERATIVE DISEASE; DISEASE COURSE; DISEASE MARKER; DISEASE SEVERITY; ENZYME ACTIVITY; ENZYME BLOOD LEVEL; FEMALE; HUMAN; HUMAN TISSUE; INFLAMMATION; LIVER; LIVER DISEASE; MALE; MOUSE; NIEMANN PICK DISEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; UPREGULATION;

BIOMARKERS; CATHEPSIN S; GENETIC DISEASES; INFLAMMATION; LYSOZYME; NEURODEGENERATION; NEUROINFLAMMATION;

ANIMALS; BETA-CYCLODEXTRINS; BRAIN; CATHEPSINS; DISEASE MODELS, ANIMAL; FEMALE; GENE DELETION; HUMANS; INFLAMMATION; LIVER; MALE; MICE; MICE, INBRED BALB C; MURAMIDASE; NIEMANN-PICK DISEASE, TYPE C; PROTEINS;

EID: 84896950203     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.526392     Document Type: Article

References (57)

1. Cappellano, G., Carecchio, M., Fleetwood, T., Magistrelli, L., Cantello, R., Dianzani, U., and Comi, C. (2013) Immunity and inflammation in neurodegenerative diseases. Am. J. Neurodegener. Dis. 2, 89-107
2. Parkinson-Lawrence, E. J., Shandala, T., Prodoehl, M., Plew, R., Borlace, G. N., and Brooks, D. A. (2010) Lysosomal storage disease: revealing lysosomal function and physiology. Physiology 25, 102-115
3. Wilms, H., Zecca, L., Rosenstiel, P., Sievers, J., Deuschl, G., and Lucius, R. (2007) Inflammation in Parkinson's diseases and other neurodegenerative diseases: cause and therapeutic implications. Curr. Pharm. Des. 13, 1925-1928 (Pubitemid 47017994)
4. Vanier, M. T. (2010) Niemann-Pick disease type C. Orphanet J. Rare Dis. 5, 16
5. Patterson, M. C., Hendriksz, C. J., Walterfang, M., Sedel, F., Vanier, M. T., Wijburg, F., and NP-C Guidelines Working Group (2012) Recommendations for the diagnosis and management of Niemann-Pick disease type C: an update. Mol. Genet. Metab. 106, 330-344
6. Garver, W. S., Francis, G. A., Jelinek, D., Shepherd, G., Flynn, J., Castro, G., Walsh Vockley, C., Coppock, D. L., Pettit, K. M., Heidenreich, R. A., and Meaney, F. J. (2007) The National Niemann-Pick C1 disease database: report of clinical features and health problems. Am. J. Med. Genet. A 143A, 1204-1211 (Pubitemid 46870076)
7. Imrie, J., Dasgupta, S., Besley, G. T., Harris, C., Heptinstall, L., Knight, S., Vanier, M. T., Fensom, A. H., Ward, C., Jacklin, E., Whitehouse, C., and Wraith, J. E. (2007) The natural history of Niemann-Pick disease type C in the UK. J. Inherit. Metab. Dis. 30, 51-59 (Pubitemid 46140226)
8. Loftus, S. K., Morris, J. A., Carstea, E. D., Gu, J. Z., Cummings, C., Brown, A., Ellison, J., Ohno, K., Rosenfeld, M. A., Tagle, D. A., Pentchev, P. G., and Pavan, W. J. (1997) Murine model of Niemann-Pick C disease: mutation in a cholesterol homeostasis gene. Science 277, 232-235 (Pubitemid 27446077)
9. Rimkunas, V. M., Graham, M. J., Crooke, R. M., and Liscum, L. (2008) In vivo antisense oligonucleotide reduction of NPC1 expression as a novel mouse model for Niemann Pick type C-associated liver disease. Hepatology 47, 1504-1512 (Pubitemid 351702734)
10. Sayre, N. L., Rimkunas, V. M., Graham, M. J., Crooke, R. M., and Liscum, L. (2010) Recovery from liver disease in a Niemann-Pick type C mouse model. J. Lipid Res. 51, 2372-2383
11. Smith, D., Wallom, K. L., Williams, I. M., Jeyakumar, M., and Platt, F. M. (2009) Beneficial effects of anti-inflammatory therapy in a mouse model of Niemann-Pick disease type C1. Neurobiol. Dis. 36, 242-251
12. Vázquez, M. C., del Pozo, T., Robledo, F. A., Carrasco, G., Pavez, L., Olivares, F., González, M., and Zanlungo, S. (2011) Alteration of gene expression profile in Niemann-Pick type C mice correlates with tissue damage and oxidative stress. PLoS One 6, e28777
13. Beltroy, E. P., Richardson, J. A., Horton, J. D., Turley, S. D., and Dietschy, J. M. (2005) Cholesterol accumulation and liver cell death in mice with Niemann-Pick type C disease. Hepatology 42, 886-893 (Pubitemid 41401127)
14. Pressey, S. N., Smith, D. A., Wong, A. M., Platt, F. M., and Cooper, J. D. (2012) Early glial activation, synaptic changes and axonal pathology in the thalamocortical system of Niemann-Pick type C1 mice. Neurobiol. Dis. 45, 1086-1100
15. Schrantz, N., Sagiv, Y., Liu, Y., Savage, P. B., Bendelac, A., and Teyton, L. (2007) The Niemann-Pick type C2 protein loads isoglobotrihexosylceramide onto CD1d molecules and contributes to the thymic selection of NKT cells. J. Exp. Med. 204, 841-852 (Pubitemid 46631613)
16. Sagiv, Y., Hudspeth, K., Mattner, J., Schrantz, N., Stern, R. K., Zhou, D., Savage, P. B., Teyton, L., and Bendelac, A. (2006) Cutting edge: impaired glycosphingolipid trafficking and NKT cell development in mice lacking Niemann-Pick type C1 protein. J. Immunol. 177, 26-30 (Pubitemid 43939110)
17. Reddy, J. V., Ganley, I. G., and Pfeffer, S. R. (2006) Clues to neuro-degeneration in Niemann-Pick type C disease from global gene expression profiling. PLoS One 1, e19
18. De Windt, A., Rai, M., Kytömäki, L., Thelen, K. M., Lütjohann, D., Bernier, L., Davignon, J., Soini, J., Pandolfo, M., and Laaksonen, R. (2007) Gene set enrichment analyses revealed several affected pathways in Niemann-pick disease type C fibroblasts. DNA Cell Biol. 26, 665-671
19. Alam, M. S., Getz, M., Safeukui, I., Yi, S., Tamez, P., Shin, J., Velázquez, P., and Haldar, K. (2012) Genomic expression analyses reveal lysosomal, innate immunity proteins, as disease correlates in murine models of a lysosomal storage disorder. PLoS One 7, e48273
20. Cluzeau, C. V., Watkins-Chow, D. E., Fu, R., Borate, B., Yanjanin, N., Dail, M. K., Davidson, C. D., Walkley, S. U., Ory, D. S., Wassif, C. A., Pavan, W. J., and Porter, F. D. (2012) Microarray expression analysis and identification of serum biomarkers for Niemann-Pick disease, type C1. Hum. Mol. Genet. 21, 3632-3646
21. Liu, B., Li, H., Repa, J. J., Turley, S. D., and Dietschy, J. M. (2008) Genetic variations and treatments that affect the lifespan of the NPC1 mouse. J. Lipid Res. 49, 663-669
22. Liu, B., Turley, S. D., Burns, D. K., Miller, A. M., Repa, J. J., and Dietschy, J. M. (2009) Reversal of defective lysosomal transport in NPC disease ameliorates liver dysfunction and neurodegeneration in the npc1-/- mouse. Proc. Natl. Acad. Sci. U.S.A. 106, 2377-2382
23. Ramirez, C. M., Liu, B., Taylor, A. M., Repa, J. J., Burns, D. K., Weinberg, A. G., Turley, S. D., and Dietschy, J. M. (2010) Weekly cyclodextrin administration normalizes cholesterol metabolism in nearly every organ of the Niemann-Pick type C1 mouse and markedly prolongs life. Pediatr. Res. 68, 309-315
24. Davidson, C. D., Ali, N. F., Micsenyi, M. C., Stephney, G., Renault, S., Dobrenis, K., Ory, D. S., Vanier, M. T., and Walkley, S. U. (2009) Chronic cyclodextrin treatment of murine Niemann-Pick C disease ameliorates neuronal cholesterol and glycosphingolipid storage and disease progression. PLoS One 4, e6951
25. Leto, G., Tumminello, F. M., Pizzolanti, G., Montalto, G., Soresi, M., Ruggeri, I., and Gebbia, N. (1996) Cathepsin D serum mass concentrations in patients with hepatocellular carcinoma and/or liver cirrhosis. Eur. J. Clin. Chem. Clin. Biochem. 34, 555-560 (Pubitemid 26258286)
26. Herszényi, L., Farinati, F., Cardin, R., István, G., Molnár, L. D., Hritz, I., De Paoli, M., Plebani, M., and Tulassay, Z. (2008) Tumor marker utility and prognostic relevance of cathepsin B, cathepsin L, urokinase-type plasminogen activator, plasminogen activator inhibitor type-1, CEA and CA 19-9 in colorectal cancer. BMC Cancer 8, 194
27. Lv, B. J., Lindholt, J. S., Cheng, X., Wang, J., and Shi, G. P. (2012) Plasma cathepsin S and cystatin C levels and risk of abdominal aortic aneurysm: a randomized population-based study. PLoS One 7, e41813
28. Ohmi, K., Kudo, L. C., Ryazantsev, S., Zhao, H. Z., Karsten, S. L., and Neufeld, E. F. (2009) Sanfilippo syndrome type B, a lysosomal storage disease, is also a tauopathy. Proc. Natl. Acad. Sci. U.S.A. 106, 8332-8337
29. Maue, R. A., Burgess, R. W., Wang, B., Wooley, C. M., Seburn, K. L., Vanier, M. T., Rogers, M. A., Chang, C. C., Chang, T. Y., Harris, B. T., Graber, D. J., Penatti, C. A., Porter, D. M., Szwergold, B. S., Henderson, L. P., Totenhagen, J. W., Trouard, T. P., Borbon, I. A., and Erickson, R. P. (2012) A novel mouse model of Niemann-Pick type C disease carrying a D1005G-Npc1 mutation comparable to commonly observed human mutations. Hum. Mol. Genet. 21, 730-750
30. Liao, G., Yao, Y., Liu, J., Yu, Z., Cheung, S., Xie, A., Liang, X., and Bi, X. (2007) Cholesterol accumulation is associated with lysosomal dysfunction and autophagic stress in Npc1 -/- mouse brain. Am. J. Pathol. 171, 962-975 (Pubitemid 47440994)
31. Amritraj, A., Peake, K., Kodam, A., Salio, C., Merighi, A., Vance, J. E., and Kar, S. (2009) Increased activity and altered subcellular distribution of lysosomal enzymes determine neuronal vulnerability in Niemann-Pick type C1-deficient mice. Am. J. Pathol. 175, 2540-2556
32. Amritraj, A., Wang, Y., Revett, T. J., Vergote, D., Westaway, D., and Kar, S. (2013) Role of cathepsin D in U18666A-induced neuronal cell death: potential implication in Niemann-Pick type C disease pathogenesis. J. Biol. Chem. 288, 3136-3152
33. 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
34. German, D. C., Liang, C. L., Song, T., Yazdani, U., Xie, C., and Dietschy, J. M. (2002) Neurodegeneration in the Niemann-Pick C mouse: glial involvement. Neuroscience 109, 437-450 (Pubitemid 34121996)
35. Liu, B., Ramirez, C. M., Miller, A. M., Repa, J. J., Turley, S. D., and Dietschy, J. M. (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
36. Grammatikakis, I., Evangelinakis, N., Salamalekis, G., Tziortzioti, V., Samaras, C., Chrelias, C., and Kassanos, D. (2009) Prevalence of severe pelvic inflammatory disease and endometriotic ovarian cysts: a 7-year retrospective study. Clin. Exp. Obstet. Gynecol. 36, 235-236
37. Ramirez, C. M., Liu, B., Aqul, A., Taylor, A. M., Repa, J. J., Turley, S. D., and Dietschy, J. M. (2011) Quantitative role of LAL, NPC2, and NPC1 in lysosomal cholesterol processing defined by genetic and pharmacological manipulations. J. Lipid Res. 52, 688-698
38. Ko, D. C., Milenkovic, L., Beier, S. M., Manuel, H., Buchanan, J., and Scott, M. P. (2005) Cell-autonomous death of cerebellar Purkinje neurons with autophagy in Niemann-Pick type C disease. PLoS Genet. 1, 81-95
39. Yu, T., and Lieberman, A. P. (2013) Npc1 acting in neurons and glia is essential for the formation and maintenance of CNS myelin. PLoS Genet. 9, e1003462
40. Taylor, A. M., Liu, B., Mari, Y., Liu, B., and Repa, J. J. (2012) Cyclodextrin mediates rapid changes in lipid balance in Npc1-/- mice without carrying cholesterol through the bloodstream. J. Lipid Res. 53, 2331-2342
41. Jiang, X., Sidhu, R., Porter, F. D., Yanjanin, N. M., Speak, A. O., te Vruchte, D. T., Platt, F. M., Fujiwara, H., Scherrer, D. E., Zhang, J., Dietzen, D. J., Schaffer, J. E., and Ory, D. S. (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
42. 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., and Ory, D. S. (2010) Cholesterol oxidation products are sensitive and specific blood-based biomarkers for Niemann-Pick C1 disease. Sci. Transl. Med. 2, 56ra81
43. Olsen, B. N., Schlesinger, P. H., Ory, D. S., and Baker, N. A. (2012) Side-chain oxysterols: from cells to membranes to molecules. Biochim. Biophys. Acta 1818, 330-336
44. Brown, A. J., and Jessup, W. (2009) Oxysterols: sources, cellular storage and metabolism, and new insights into their roles in cholesterol homeostasis. Mol. Aspects Med. 30, 111-122
45. Hughes, T. M., Rosano, C., Evans, R. W., and Kuller, L. H. (2013) Brain cholesterol metabolism, oxysterols, and dementia. J. Alzheimers Dis. 33, 891-911
46. Leoni, V., and Caccia, C. (2011) Oxysterols as biomarkers in neurodegenerative diseases. Chem. Phys. Lipids 164, 515-524
47. Pišlar, A., and Kos, J. (2013) Cysteine cathepsins in neurological disorders. Mol. Neurobiol. 10.1007/s12035-013-8576-6
48. Nakanishi, H. (2003) Microglial functions and proteases. Mol. Neurobiol. 27, 163-176
49. Kelly, D. A., Portmann, B., Mowat, A. P., Sherlock, S., and Lake, B. D. (1993) Niemann-Pick disease type C: diagnosis and outcome in children, with particular reference to liver disease. J. Pediatr. 123, 242-247 (Pubitemid 23221104)
50. Yerushalmi, B., Sokol, R. J., Narkewicz, M. R., Smith, D., Ashmead, J. W., and Wenger, D. A. (2002) Niemann-pick disease type C in neonatal cholestasis at a North American Center. J. Pediatr. Gastroenterol. Nutr. 35, 44-50 (Pubitemid 34778755)
51. Trexler, A. J., and Nilsson, M. R. (2007) The formation of amyloid fibrils from proteins in the lysozyme family. Curr. Protein Pept. Sci. 8, 537-557 (Pubitemid 351266988)
52. Vieira, M. N., Forny-Germano, L., Saraiva, L. M., Sebollela, A., Martinez, A. M., Houzel, J. C., De Felice, F. G., and Ferreira, S. T. (2007) Soluble oligomers from a non-disease related protein mimic Aβ-induced tau hyperphosphorylation and neurodegeneration. J. Neurochem. 103, 736-748 (Pubitemid 47498038)
53. Vitner, E. B., Platt, F. M., and Futerman, A. H. (2010) Common and uncommon pathogenic cascades in lysosomal storage diseases. J. Biol. Chem. 285, 20423-20427
54. Cologna, S. M., Cluzeau, C. V., Yanjanin, N. M., Blank, P. S., Dail, M. K., Siebel, S., Toth, C. L., Wassif, C. A., Lieberman, A. P., and Porter, F. D. (2014) Human and mouse neuroinflammation markers in Niemann-Pick disease, type C1. J. Inherit. Metab. Dis. 37, 83-92
55. Vitner, E. B., Dekel, H., Zigdon, H., Shachar, T., Farfel-Becker, T., Eilam, R., Karlsson, S., and Futerman, A. H. (2010) Altered expression and distribution of cathepsins in neuronopathic forms of Gaucher disease and in other sphingolipidoses. Hum. Mol. Genet. 19, 3583-3590
56. Hruz, T., Wyss, M., Docquier, M., Pfaffl, M. W., Masanetz, S., Borghi, L., Verbrugghe, P., Kalaydjieva, L., Bleuler, S., Laule, O., Descombes, P., Gruissem, W., and Zimmermann, P. (2011) RefGenes: identification of reliable and condition specific reference genes for RT-qPCR data normalization. BMC Genomics 12, 156
57. Repa, J. J., Li, H., Frank-Cannon, T. C., Valasek, M. A., Turley, S. D., Tansey, M. G., and Dietschy, J. M. (2007) Liver X receptor activation enhances cholesterol loss from the brain, decreases neuroinflammation, and increases survival of the NPC1 mouse. J. Neurosci. 27, 14470-14480