Viable Neuronopathic Gaucher Disease Model in Medaka (Oryzias latipes) Displays Axonal Accumulation of Alpha-Synuclein

PLoS Genetics

Volumn 11, Issue 4, 2015, Pages

  Uemura, Norihito ^a   Koike, Masato ^b   Ansai, Satoshi ^c   Kinoshita, Masato ^c   Ishikawa Fujiwara, Tomoko ^d   Matsui, Hideaki ^a,h   Naruse, Kiyoshi ^e   Sakamoto, Naoaki ^f   Uchiyama, Yasuo ^b   Todo, Takeshi ^d   Takeda, Shunichi ^a,g   Yamakado, Hodaka ^a,g   Takahashi, Ryosuke ^a,g  

^a KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b JUNTENDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c KYOTO UNIVERSITY   (Japan)

^d OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^e NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

^f HIROSHIMA UNIVERSITY   (Japan)

^g JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^h UNIVERSITY OF MIYAZAKI   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; GLUCOSYLCERAMIDASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGOSOME; CELL INFILTRATION; CELL LOSS; CONTROLLED STUDY; GAUCHER DISEASE; GLIOSIS; GLUCOCEREBROSIDASE GENE; LONG TERM SURVIVAL; LYSOSOME; NERVE FIBER DEGENERATION; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; NONSENSE MUTATION; ORYZIAS LATIPES; PARKINSON DISEASE; PATHOGENESIS; ANIMAL; AXON; DEFICIENCY; DISEASE MODEL; GENETICS; METABOLISM; ORYZIAS; PATHOLOGY; PHAGOSOME; ULTRASTRUCTURE;

MUS; ORYZIAS LATIPES; ORYZIINAE;

ALPHA-SYNUCLEIN; ANIMALS; AXONS; DISEASE MODELS, ANIMAL; GAUCHER DISEASE; GLUCOSYLCERAMIDASE; ORYZIAS; PHAGOSOMES;

EID: 84930318487     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005065     Document Type: Article

References (62)

1. Futerman AH, Zimran A, (2006) Gaucher disease: CRC Press.
2. Grabowski GA, (2008) Phenotype, diagnosis, and treatment of Gaucher's disease. Lancet 372: 1263–1271. doi: 10.1016/S0140-6736(08)61522-6 19094956
3. Wong K, Sidransky E, Verma A, Mixon T, Sandberg GD, et al. (2004) Neuropathology provides clues to the pathophysiology of Gaucher disease. Mol Genet Metab 82: 192–207. 15234332
4. Eblan MJ, Goker-Alpan O, Sidransky E, (2005) Perinatal lethal Gaucher disease: a distinct phenotype along the neuronopathic continuum. Fetal Pediatr Pathol 24: 205–222. 16396828
5. Neumann J, Bras J, Deas E, O'Sullivan SS, Parkkinen L, et al. (2009) Glucocerebrosidase mutations in clinical and pathologically proven Parkinson's disease. Brain 132: 1783–1794. doi: 10.1093/brain/awp044 19286695
6. Sidransky E, Nalls MA, Aasly JO, Aharon-Peretz J, Annesi G, et al. (2009) Multicenter analysis of glucocerebrosidase mutations in Parkinson's disease. N Engl J Med 361: 1651–1661. doi: 10.1056/NEJMoa0901281 19846850
7. Bultron G, Kacena K, Pearson D, Boxer M, Yang R, et al. (2010) The risk of Parkinson's disease in type 1 Gaucher disease. J Inherit Metab Dis 33: 167–173. doi: 10.1007/s10545-010-9055-0 20177787
8. Manning-Bog AB, Schule B, Langston JW, (2009) Alpha-synuclein-glucocerebrosidase interactions in pharmacological Gaucher models: a biological link between Gaucher disease and parkinsonism. Neurotoxicology 30: 1127–1132. doi: 10.1016/j.neuro.2009.06.009 19576930
9. Mazzulli JR, Xu YH, Sun Y, Knight AL, McLean PJ, et al. (2011) Gaucher disease glucocerebrosidase and alpha-synuclein form a bidirectional pathogenic loop in synucleinopathies. Cell 146: 37–52. doi: 10.1016/j.cell.2011.06.001 21700325
10. Sardi SP, Clarke J, Kinnecom C, Tamsett TJ, Li L, et al. (2011) 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 108: 12101–12106. doi: 10.1073/pnas.1108197108 21730160
11. Xu YH, Sun Y, Ran H, Quinn B, Witte D, et al. (2011) Accumulation and distribution of alpha-synuclein and ubiquitin in the CNS of Gaucher disease mouse models. Mol Genet Metab 102: 436–447. doi: 10.1016/j.ymgme.2010.12.014 21257328
12. Schondorf DC, Aureli M, McAllister FE, Hindley CJ, Mayer F, et al. (2014) iPSC-derived neurons from GBA1-associated Parkinson's disease patients show autophagic defects and impaired calcium homeostasis. Nat Commun 5: 4028. doi: 10.1038/ncomms5028 24905578
13. Gegg ME, Burke D, Heales SJ, Cooper JM, Hardy J, et al. (2012) Glucocerebrosidase deficiency in substantia nigra of parkinson disease brains. Ann Neurol 72: 455–463. doi: 10.1002/ana.23614 23034917
14. Sardi SP, Singh P, Cheng SH, Shihabuddin LS, Schlossmacher MG, (2012) Mutant GBA1 expression and synucleinopathy risk: first insights from cellular and mouse models. Neurodegener Dis 10: 195–202. doi: 10.1159/000335038 22327140
15. Murphy KE, Gysbers AM, Abbott SK, Tayebi N, Kim WS, et al. (2014) Reduced glucocerebrosidase is associated with increased alpha-synuclein in sporadic Parkinson's disease. Brain 137: 834–848. doi: 10.1093/brain/awt367 24477431
16. Wittbrodt J, Shima A, Schartl M, (2002) Medaka—a model organism from the far East. Nat Rev Genet 3: 53–64. 11823791
17. Taniguchi Y, Takeda S, Furutani-Seiki M, Kamei Y, Todo T, et al. (2006) Generation of medaka gene knockout models by target-selected mutagenesis. Genome Biol 7: R116. 17156454
18. Ansai S, Kinoshita M, (2014) Targeted mutagenesis using CRISPR/Cas system in medaka. Biol Open 3: 362–371. doi: 10.1242/bio.20148177 24728957
19. Ansai S, Sakuma T, Yamamoto T, Ariga H, Uemura N, et al. (2013) Efficient targeted mutagenesis in medaka using custom-designed transcription activator-like effector nucleases. Genetics 193: 739–749. doi: 10.1534/genetics.112.147645 23288935
20. Kinoshita M, Kani S, Ozato K, Wakamatsu Y, (2000) Activity of the medaka translation elongation factor 1alpha-A promoter examined using the GFP gene as a reporter. Dev Growth Differ 42: 469–478. 11041488
21. Ansai S, Ochiai H, Kanie Y, Kamei Y, Gou Y, et al. (2012) Targeted disruption of exogenous EGFP gene in medaka using zinc-finger nucleases. Dev Growth Differ 54: 546–556. doi: 10.1111/j.1440-169X.2012.01357.x 22642582
22. Matsui H, Gavinio R, Asano T, Uemura N, Ito H, et al. (2013) PINK1 and Parkin complementarily protect dopaminergic neurons in vertebrates. Hum Mol Genet 22: 2423–2434. doi: 10.1093/hmg/ddt095 23449626
23. Matsui H, Sato F, Sato S, Koike M, Taruno Y, et al. (2013) ATP13A2 deficiency induces a decrease in cathepsin D activity, fingerprint-like inclusion body formation, and selective degeneration of dopaminergic neurons. FEBS Lett 587: 1316–1325. doi: 10.1016/j.febslet.2013.02.046 23499937
24. Ishikawa T, Kamei Y, Otozai S, Kim J, Sato A, et al. (2010) High-resolution melting curve analysis for rapid detection of mutations in a Medaka TILLING library. BMC Mol Biol 11: 70. doi: 10.1186/1471-2199-11-70 20840787
25. Tayebi N, Cushner SR, Kleijer W, Lau EK, Damschroder-Williams PJ, et al. (1997) Prenatal lethality of a homozygous null mutation in the human glucocerebrosidase gene. Am J Med Genet 73: 41–47. 9375921
26. Tybulewicz VL, Tremblay ML, LaMarca ME, Willemsen R, Stubblefield BK, et al. (1992) Animal model of Gaucher's disease from targeted disruption of the mouse glucocerebrosidase gene. Nature 357: 407–410. 1594045
27. Enquist IB, Lo Bianco C, Ooka A, Nilsson E, Mansson JE, et al. (2007) Murine models of acute neuronopathic Gaucher disease. Proc Natl Acad Sci U S A 104: 17483–17488. 17954912
28. Pennelli N, Scaravilli F, Zacchello F, (1969) The morphogenesis of Gaucher cells investigated by electron microscopy. Blood 34: 331–347. 5804023
29. Sun Y, Quinn B, Witte DP, Grabowski GA, (2005) Gaucher disease mouse models: point mutations at the acid beta-glucosidase locus combined with low-level prosaposin expression lead to disease variants. J Lipid Res 46: 2102–2113. 16061944
30. Peri F, Nusslein-Volhard C, (2008) Live imaging of neuronal degradation by microglia reveals a role for v0-ATPase a1 in phagosomal fusion in vivo. Cell 133: 916–927. doi: 10.1016/j.cell.2008.04.037 18510934
31. Baumgart EV, Barbosa JS, Bally-Cuif L, Gotz M, Ninkovic J, (2012) Stab wound injury of the zebrafish telencephalon: a model for comparative analysis of reactive gliosis. Glia 60: 343–357. doi: 10.1002/glia.22269 22105794
32. Farfel-Becker T, Vitner EB, Pressey SN, Eilam R, Cooper JD, et al. (2011) Spatial and temporal correlation between neuron loss and neuroinflammation in a mouse model of neuronopathic Gaucher disease. Hum Mol Genet 20: 1375–1386. doi: 10.1093/hmg/ddr019 21252206
33. Rink E, Wullimann MF, (2001) The teleostean (zebrafish) dopaminergic system ascending to the subpallium (striatum) is located in the basal diencephalon (posterior tuberculum). Brain Res 889: 316–330. 11166725
34. Sun Y, Liou B, Ran H, Skelton MR, Williams MT, et al. (2010) Neuronopathic Gaucher disease in the mouse: viable combined selective saposin C deficiency and mutant glucocerebrosidase (V394L) mice with glucosylsphingosine and glucosylceramide accumulation and progressive neurological deficits. Hum Mol Genet 19: 1088–1097. doi: 10.1093/hmg/ddp580 20047948
35. Vitner EB, Dekel H, Zigdon H, Shachar T, Farfel-Becker T, et al. (2010) Altered expression and distribution of cathepsins in neuronopathic forms of Gaucher disease and in other sphingolipidoses. Hum Mol Genet 19: 3583–3590. doi: 10.1093/hmg/ddq273 20616152
36. Cuoghi B, Mola L, (2007) Microglia of teleosts: facing a challenge in neurobiology. Eur J Histochem 51: 231–240. 18162452
37. Fujimori KE, Kawasaki T, Deguchi T, Yuba S, (2008) Characterization of a nervous system-specific promoter for growth-associated protein 43 gene in Medaka (Oryzias latipes). Brain Res 1245: 1–15. doi: 10.1016/j.brainres.2008.09.071 18951884
38. Dawson TM, Ko HS, Dawson VL, (2010) Genetic animal models of Parkinson's disease. Neuron 66: 646–661. doi: 10.1016/j.neuron.2010.04.034 20547124
39. Hirsch EC, Hunot S, (2009) Neuroinflammation in Parkinson's disease: a target for neuroprotection? Lancet Neurol 8: 382–397. doi: 10.1016/S1474-4422(09)70062-6 19296921
40. Kim C, Ho DH, Suk JE, You S, Michael S, et al. (2013) Neuron-released oligomeric alpha-synuclein is an endogenous agonist of TLR2 for paracrine activation of microglia. Nat Commun 4: 1562. doi: 10.1038/ncomms2534 23463005
41. Abeliovich A, Schmitz Y, Farinas I, Choi-Lundberg D, Ho WH, et al. (2000) Mice lacking alpha-synuclein display functional deficits in the nigrostriatal dopamine system. Neuron 25: 239–252. 10707987
42. Farfel-Becker T, Vitner EB, Futerman AH, (2011) Animal models for Gaucher disease research. Dis Model Mech 4: 746–752. doi: 10.1242/dmm.008185 21954067
43. Holleran WM, Ginns EI, Menon GK, Grundmann JU, Fartasch M, et al. (1994) Consequences of beta-glucocerebrosidase deficiency in epidermis. Ultrastructure and permeability barrier alterations in Gaucher disease. J Clin Invest 93: 1756–1764. 8163674
44. Murayama E, Kissa K, Zapata A, Mordelet E, Briolat V, et al. (2006) Tracing hematopoietic precursor migration to successive hematopoietic organs during zebrafish development. Immunity 25: 963–975. 17157041
45. Lieberman AP, Puertollano R, Raben N, Slaugenhaupt S, Walkley SU, et al. (2012) Autophagy in lysosomal storage disorders. Autophagy 8: 719–730. doi: 10.4161/auto.19469 22647656
46. Liao G, Yao Y, Liu J, Yu Z, Cheung S, et al. (2007) Cholesterol accumulation is associated with lysosomal dysfunction and autophagic stress in Npc1 -/- mouse brain. Am J Pathol 171: 962–975. 17631520
47. Koike M, Shibata M, Waguri S, Yoshimura K, Tanida I, et al. (2005) Participation of autophagy in storage of lysosomes in neurons from mouse models of neuronal ceroid-lipofuscinoses (Batten disease). Am J Pathol 167: 1713–1728. 16314482
48. Maday S, Wallace KE, Holzbaur EL, (2012) Autophagosomes initiate distally and mature during transport toward the cell soma in primary neurons. J Cell Biol 196: 407–417. doi: 10.1083/jcb.201106120 22331844
49. Lee S, Sato Y, Nixon RA, (2011) Lysosomal proteolysis inhibition selectively disrupts axonal transport of degradative organelles and causes an Alzheimer's-like axonal dystrophy. J Neurosci 31: 7817–7830. doi: 10.1523/JNEUROSCI.6412-10.2011 21613495
50. Friedman LG, Lachenmayer ML, Wang J, He L, Poulose SM, et al. (2012) Disrupted autophagy leads to dopaminergic axon and dendrite degeneration and promotes presynaptic accumulation of alpha-synuclein and LRRK2 in the brain. J Neurosci 32: 7585–7593. doi: 10.1523/JNEUROSCI.5809-11.2012 22649237
51. Orimo S, Uchihara T, Nakamura A, Mori F, Kakita A, et al. (2008) Axonal alpha-synuclein aggregates herald centripetal degeneration of cardiac sympathetic nerve in Parkinson's disease. Brain 131: 642–650. 18079166
52. Anheim M, Elbaz A, Lesage S, Durr A, Condroyer C, et al. (2012) Penetrance of Parkinson disease in glucocerebrosidase gene mutation carriers. Neurology 78: 417–420. doi: 10.1212/WNL.0b013e318245f476 22282650
53. Dauer W, Kholodilov N, Vila M, Trillat AC, Goodchild R, et al. (2002) Resistance of alpha-synuclein null mice to the parkinsonian neurotoxin MPTP. Proc Natl Acad Sci U S A 99: 14524–14529. 12376616
54. Paine SM, Anderson G, Bedford K, Lawler K, Mayer RJ, et al. (2013) Pale body-like inclusion formation and neurodegeneration following depletion of 26S proteasomes in mouse brain neurones are independent of alpha-synuclein. PLoS One 8: e54711. doi: 10.1371/journal.pone.0054711 23382946
55. Ochiai H, Sakamoto N, Suzuki K, Akasaka K, Yamamoto T, (2008) The Ars insulator facilitates I-SceI meganuclease-mediated transgenesis in the sea urchin embryo. Dev Dyn 237: 2475–2482. doi: 10.1002/dvdy.21690 18729225
56. Takagi H, Inai Y, Watanabe S, Tatemoto S, Yajima M, et al. (2012) Nucleosome exclusion from the interspecies-conserved central AT-rich region of the Ars insulator. J Biochem 151: 75–87. doi: 10.1093/jb/mvr118 21930654
57. Emelyanov A, Gao Y, Naqvi NI, Parinov S, (2006) Trans-kingdom transposition of the maize dissociation element. Genetics 174: 1095–1104. 16951067
58. Ansai S, Inohaya K, Yoshiura Y, Schartl M, Uemura N, et al. (2014) Design, evaluation, and screening methods for efficient targeted mutagenesis with transcription activator-like effector nucleases in medaka. Dev Growth Differ 56: 98–107. doi: 10.1111/dgd.12104 24286287
59. Bielawski J, Pierce JS, Snider J, Rembiesa B, Szulc ZM, et al. (2010) Sphingolipid analysis by high performance liquid chromatography-tandem mass spectrometry (HPLC-MS/MS). Adv Exp Med Biol 688: 46–59. 20919645
60. Matsui H, Taniguchi Y, Inoue H, Kobayashi Y, Sakaki Y, et al. (2010) Loss of PINK1 in medaka fish (Oryzias latipes) causes late-onset decrease in spontaneous movement. Neurosci Res 66: 151–161. doi: 10.1016/j.neures.2009.10.010 19895857
61. Lee BR, Kamitani T, (2011) Improved immunodetection of endogenous alpha-synuclein. PLoS One 6: e23939. doi: 10.1371/journal.pone.0023939 21886844
62. Koike M, Nakanishi H, Saftig P, Ezaki J, Isahara K, et al. (2000) Cathepsin D deficiency induces lysosomal storage with ceroid lipofuscin in mouse CNS neurons. J Neurosci 20: 6898–6906. 10995834