Visualization of active glucocerebrosidase in rodent brain with high spatial resolution following in situ labeling with fluorescent activity based probes

PLoS ONE

Volumn 10, Issue 9, 2015, Pages

  Chao, Daniela Herrera Moro ^a   Kallemeijn, Wouter W ^a,e   Marques, Andre R A ^a   Orre, Marie ^b   Ottenhoff, Roelof ^a   Van Roomen, Cindy ^a   Foppen, Ewout ^a   Renner, Maria C ^b   Moeton, Martina ^b   Van Eijk, Marco ^e   Boot, Rolf G ^e   Kamphuis, Willem ^b   Hol, Elly M ^b,c,d   Aten, Jan ^a   Overkleeft, Hermen S ^e   Kalsbeek, Andries ^a,b   Aerts, Johannes M F G ^e  

^a ACADEMIC MEDICAL CENTER   (Netherlands)

^b NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^d UNIVERSITY OF AMSTERDAM   (Netherlands)

^e LEIDEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

AZIRIDINE; BRAIN ENZYME; CYCLOPHELLITOL; FLUORESCENT DYE; GLUCOSYLCERAMIDASE; PROTEIN GBA2; UNCLASSIFIED DRUG; GLUCOSYLCERAMIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; BIOCHEMICAL ANALYSIS; BRAIN SLICE; BRAIN STEM; CEREBELLAR ATAXIA; CEREBELLUM CORTEX; CONTROLLED STUDY; DEGENERATIVE DISEASE; ENZYME ANALYSIS; GEL ELECTROPHORESIS; IN VIVO STUDY; MALE; MOTOR CONTROL; NONHUMAN; PROTEIN CONTENT; PROTEIN LOCALIZATION; RAT; RODENT; ANIMAL; ASTROCYTE; BRAIN; C57BL MOUSE; CELL CULTURE; CHEMISTRY; CONFOCAL MICROSCOPY; ENZYMOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; GAUCHER DISEASE; GENETICS; METABOLISM; MICROGLIA; MOUSE; PATHOLOGY; PURKINJE CELL; WISTAR RAT;

ANIMALS; ASTROCYTES; BRAIN; CELLS, CULTURED; CEREBELLAR ATAXIA; FLUORESCENT ANTIBODY TECHNIQUE; FLUORESCENT DYES; GAUCHER DISEASE; GLUCOSYLCERAMIDASE; GLUCOSYLCERAMIDES; MALE; MICE; MICE, INBRED C57BL; MICROGLIA; MICROSCOPY, CONFOCAL; NEURODEGENERATIVE DISEASES; PURKINJE CELLS; RATS; RATS, WISTAR;

EID: 84947983376     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0138107     Document Type: Article

References (47)

1. Beutler E, Grabowski GA. Gaucher disease, The Metabolic and Molecular Bases of Inherited Disease (8th ed.). New York: Scriver CR, Sly WS, Valle D. (Eds.), McGraw-Hill, 2001; 3635-3668.
2. van Weely S, Brandsma M, Strijland A, Tager JM, Aerts JM. Demonstration of the existence of a second, non-lysosomal glucocerebrosidase that is not deficient in Gaucher disease. Biochim Biophys Acta 1993; 1181:55-62. PMID: 8457606
3. Xu YH, Sun Y, Ran H, Quinn B, Witte D, Grabowski GA. Accumulation and distribution of osynuclein andubiquitin in the CNS of Gaucher disease mouse models. Mol Genet Metab 2011; 102:436-447. doi: 10.1016/j.ymgme.2010.12.014 PMID: 21257328
4. Wong K, Sidransky E, Verma A, Mixon T, Sandberg GD, Wakefield LK, et al. Neuropathology provides clues to the pathophysiology of Gaucher disease. Mol Genet Metab 2004; 82:192-207. PMID: 15234332
5. Westbroek W, Gustafson AM, Sidransky E. Exploring the link between glucocerebrosidase mutations and Parkinsonism. Trends Mol Med 2011; 17:485-93. doi: 10.1016/j.molmed.2011.05.003 PMID: 21723784
6. Gegg ME, Burke D, Heales SJ, Cooper JM, Hardy J, Wood NW, et al. Glucocerebrosidase deficiency in substantia nigra of Parkinson disease brains. Ann Neurol 2012; 72:455-463. doi: 10.1002/ana.23614 PMID: 23034917
7. Lwin A, Orvisky E, Goker-Alpan O, LaMarca ME, Sidransky E. Glucocerebrosidase mutations in subjects with Parkinsonism. Mol Genet Metab 2004; 81: 70-73. PMID: 14728994
8. Siebert M, Sidransky E, Westbroek W. Glucocerebrosidase is shaking up the synucleinopathies. Brain 2014; 137:1304-22. doi: 10.1093/brain/awu002 PMID: 24531622
9. Schapira AH. Glucocerebrosidase and Parkinson disease: Recent advances. Mol Cell Neurosci. 2015; pii: S1044-7431(15)00042-1.
10. Sardi SP, Cheng SH, Shihabuddin LS. Gaucher-relatedsynucleinopathies: the examination of sporadic neurodegenerationfroma rare (disease) angle. Prog Neurobiol. 2015; 125:47-62. doi: 10.1016/j.pneurobio.2014.12.001 PMID: 25573151
11. Manning-Boʇ AB, Schüle B, Langston JW. Alpha-synuclein-glucocerebrosidase interactions in pharmacological Gaucher models: A biological link between Gaucher disease and parkinsonism. Neurotoxicology 2009; 30:1127-32. doi: 10.1016/j.neuro.2009.06.009 PMID: 19576930
12. Mazzulli JR, Xu YH, Sun Y, Knight AL, McLean PJ, Sydransky E, et al. Gaucher disease glucocerebrosidase and osynuclein form a bidirectional pathogenic loop in synucleinopathies. Cell 2011; 146:37-52. doi: 10.1016/j.cell.2011.06.001 PMID: 21700325
13. Sardi SP, Clarke J, Kinnecom C, Tamsett TJ, Li L, Passini MA, et al. CNS expression of glucocerebrosidase corrects alpha-synuclein pathology and memory in a mouse model of Gaucher-related synucleinopathy. Proc Natl Acad Sci U S A 2011; 108:12101-106. doi: 10.1073/pnas.1108197108 PMID: 21730160
14. Sardi SP, Singh P, Cheng SH, Shihabuddin LS, Schlossmacher MG. Mutant GBA1 expression and synucleinopathy risk: first insights from cellular and mouse models. Neurodegener Dis 2012; 10:195-202. doi: 10.1159/000335038 PMID: 22327140
15. Reczek D, Schwake M, Schröder J, Hughes H, Blanz J, Jin X, et al. LIMP-2 is a receptor for lysosomalmannose-6-phosphate-independent targeting of beta-glucocerebrosidase. Cell. 2007; 131:770-83. PMID: 18022370
16. Rothaug M, Zunke F, Mazzulli JR, Schweizer M, Altmeppen H, Altmeppen H, et al. LIMP-2 expression is critical for β-glucocerebrosidase activity and osynuclein clearance. Proc Natl Acad Sci U S A 2014; 111:15573-8. doi: 10.1073/pnas.1405700111 PMID: 25316793
17. Barton NW, Brady RO, Dambrosia JM, Di Bisceglie AM, Doppelt SH, Hill SC, et al. Replacement therapy for inherited enzyme deficiency-macrophage-targeted glucocerebrosidase for Gaucher's disease. N Engl J Med 1991; 324:1464-70. PMID: 2023606
18. Cox T, Lachmann R, Hollak C, Aerts J, van Weely S, Hrebícek M, et al. Novel oral treatment of Gaucher's disease with N-butyldeoxynojirimycin (OGT 918) to decrease substrate biosynthesis. Lancet. 2000; 355:1481-5. PMID: 10801168
19. Poole RM. Eliglustat: first global approval. Drugs. 2014; 74(15):1829-36. doi: 10.1007/s40265-014-0296-3 PMID: 25239269
20. Ghisaidoobe AT, van den Berg RJ, Butt SS, Strijland A, Donker-Koopman WE, Scheij S, et al. Identification and development of biphenyl substituted iminosugars as improved dual glucosylceramide synthase/neutral glucosylceramidase inhibitors. J Med Chem. 2014; 57:9096-104. doi: 10.1021/jm501181z PMID: 25250725
21. Witte MD, Kallemeijn WW, Aten J, Li KY, Strijland A, Donker-Koopman WE, et al. Ultrasensitive in situ visualization of active glucocerebrosidase molecules. Nat Chem Biol 2010; 6:907-13. doi: 10.1038/nchembio.466 PMID: 21079602
22. Aerts JM, Kallemeijn WW, Wegdam W, Joao Ferraz M, van Breemen MJ, Dekker N, et al. Biomarkers in the diagnosis of lysosomal storage disorders: proteins, lipids, and inhibodies. J Inherit Metab Dis 2011; 34:605-19. doi: 10.1007/s10545-011-9308-6 PMID: 21445610
23. Kallemeijn WW, Li KY, Witte MD, Marques AR, Aten J, Scheij S, et al. Novel activity-based probes for broad-spectrum profiling of retaining β-exoglucosidases in situ and in vivo. Angew Chem Int Ed Engl 2012; 51:12529-33. doi: 10.1002/anie.201207771 PMID: 23139194
24. Kallemeijn WW, Witte MD, Wennekes T, Aerts JM. Mechanism-based inhibitors of glycosidases: design and applications. Adv Carbohydr Chem Biochem. 2014; 71:297-338. doi: 10.1016/B978-0-12-800128-8.00004-2 PMID: 25480507
25. Li KY, Jiang J, Witte MD, Kallemeijn WW, Donker-Koopman WE, Boot RG, et al. Exploring functional cyclophellitol analogues as human retaining beta-glucosidase inhibitors. Org Biomol Chem. 2014; 12: 7786-91. doi: 10.1039/c4ob01611d PMID: 25156485
26. Willems LI, Jiang J, Li KY, Witte MD, Kallemeijn WW, Beenaker TJ, et al. From covalent glycosidase inhibitors to activity-based glycosidase probes. Chemistry. 2014; 20:10864-72. doi: 10.1002/chem. 201404014 PMID: 25100671
27. Kallemeijn WW, Witte MD, Voorn-Brouwer TM, Walvoort MT, Li KY, Codée JD, et al. A sensitive gelbased method combining distinct cyclophellitol-based probes for the identification of acid/base residues in human retaining β-glucosidases. J Biol Chem. 2014; 289:35351-62. doi: 10.1074/jbc.M114.593376 PMID: 25344605
28. Jiang J, Kallemeijn WW, Wright DW, vanden Nieuwendijk AMCH, Rohde VC, et al. In vitro and in vivo comparative and competitive activity-based protein profiling of GH29 α-L-fucosidases. Chem Sci. 2015; 6: 2782-9.
29. Aerts JM, Donker-Koopman WE, van der Vliet MK, Jonsson LM, Ginns EI, Murray GJ, et al. The occurrence of two immunologically distinguishable beta-glucocerebrosidases in human spleen. Eur J Biochem. 1985; 150:565-74. PMID: 4018098
30. Orre M, Kamphuis W, Osborn LM, Melief J, Kooijman L, Huitinga I, et al. Acute isolation and transcriptome characterization of cortical astrocytes and microglia from young and aged mice. Neurobiol Aging 2014; 35:1-14. doi: 10.1016/j.neurobiolaging.2013.07.008 PMID: 23954174
31. Karssen AM, Meijer OC, Pons D, De Kloet ER. Localization of mRNA expression of P-glycoprotein at the blood-brain barrier and in the hippocampus. Ann NY Acad Sci 2004; 1032:308-311. PMID: 15677438
32. Maries E, Dass B, Collier TJ, Kordower JH, Steece-Collier K. The role of alpha-synuclein in Parkinson's disease: insights from animal models. Nat Rev Neurosci 2003; 4:727-738. PMID: 12951565
33. Yap TL, Gruschus JM, Velayati A, Westbroek W, Goldin E, Moaven N, et al. Alpha-synuclein interacts with Glucocerebrosidase providing a molecular link between Parkinson and Gaucher diseases. J Biol Chem2011; 286:28080-8. doi: 10.1074/jbc.M111.237859 PMID: 21653695
34. Goker-Alpan O, Stubblefield BK, Giasson BI, Sidransky E. Glucocerebrosidase is present in α-synuclein inclusions in Lewy body disorders. Acta Neuropathol 2010; 120:641-649. doi: 10.1007/s00401-010-0741-7 PMID: 20838799
35. Ron I, Rapaport D, Horowitz M. Interaction between parkin and mutant glucocerebrosidase variants: A possible link between Parkinson disease and Gaucher disease. Hum Mol Genet 2010; 19:3771-378. doi: 10.1093/hmg/ddq292 PMID: 20643691
36. Nordström V, Willershäuser M, Herzer S, Rozman J, von Bohlen Und Halbach O, Meldner S, et al. Neuronal expression of glucosylceramide synthase in central nervous system regulates body weight and energy homeostasis. PLoS Biol 2013; 11:e1001506. doi: 10.1371/journal.pbio.1001506 PMID: 23554574
37. Gao S, Zhu G, Gao X, Wu D, Carrasco P, Casals N, et al. Important roles of brain-specific carnitine palmitoyltransferase and ceramidemetabolism in leptin hypothalamic control of feeding. Proc Natl Acad Sci U S A 2011; 108: 9691-9696. doi: 10.1073/pnas.1103267108 PMID: 21593415
38. Ramírez S, Martins L, Jacas J, Carrasco P, Pozo M, Clotet J, et al. Hypothalamicceramide levels regulated by CPT1C mediate the orexigenic effect of ghrelin. Diabetes 2013; 62:2329-2337. doi: 10.2337/db12-1451 PMID: 23493572
39. Vitner EB, Salomon R, Farfel-Becker T, Meshcheriakova A, Ali M, Klein AD, et al. RIPK3 as a potential therapeutic target for Gaucher's disease. Nat Med 2014; 20:204-208. doi: 10.1038/nm.3449 PMID: 24441827
40. Farfel-Becker T, Vitner EB, Kelly SL, Bame JR, Duan J, Shinder V, et al. Neuronal accumulation of glucosylceramide in a mouse model of neuronopathic Gaucher disease leads to neurodegeneration. Hum Mol Genet 2014; 23:843-54. doi: 10.1093/hmg/ddt468 PMID: 24064337
41. Yildiz Y, Matern H, Thompson B, Allegood JC, Warren RL, Ramirez DM, et al. Mutation of beta-glucosidase 2 causes glycolipid storage disease and impaired male fertility. J Clin Invest. 2006; 116:2985-94. PMID: 17080196
42. Boot RG, Verhoek M, Donker-Koopman W, Strijland A, van Marle J, Overkleeft HS, et al. Identification of the non-lysosomal glucosylceramidase as beta-glucosidase2. J Biol Chem 2007; 282:1305-1312. PMID: 17105727
43. Hammer MB, Eleuch-Fayache G, Schottlaender LV, Nehdi H, Gibbs JR, Arepalli SK, et al. Mutations in GBA2 cause autosomal-recessive cerebellar ataxia with spasticity. Am J Hum Genet 2013; 92: 245-251. doi: 10.1016/j.ajhg.2012.12.012 PMID: 23332917
44. Martin E, Schüle R, Smets K, Rastetter A, Boukhris A, Loureiro JL, et al. Loss of function of glucocerebrosidase GBA2 is responsible for motor neuron defects in hereditary spastic paraplegia. Am J Hum Genet 2013; 92:238-244. doi: 10.1016/j.ajhg.2012.11.021 PMID: 23332916
45. Wakabayashi K, Hayashi S, Yoshimoto M, Kudo H, Takahashi H. NACP/alpha-synuclein-positive filamentous inclusions in astrocytes and oligodendrocytes of Parkinson's disease brains. Acta Neuropathol 2000; 99:14-20. PMID: 10651022
46. Sekiyama K, Sugama S, Fujita M, Sekigawa A, Takamatsu Y, Waragai M, et al. Neuroinflammation in Parkinson's Disease and Related Disorders: A Lesson from Genetically Manipulated Mouse Models of α-Synucleinopathies. Parkinsons Dis 2012; 271732.
47. Vitner EB, Farfel-Becker T, Eilam R, Biton I, Futerman AH. Contribution of brain inflammation to neuronal cell death in neuronopathic forms of Gaucher's disease. Brain 2012; 135:1724-1735. doi: 10.1093/brain/aws095 PMID: 22566609