Loss of function of glucocerebrosidase GBA2 is responsible for motor neuron defects in hereditary spastic paraplegia

American Journal of Human Genetics

Volumn 92, Issue 2, 2013, Pages 238-244

  Martin, Elodie ^a,b,c,d   Schüle, Rebecca ^e   Smets, Katrien ^f,g,h   Rastetter, Agnès ^a,b,c,d   Boukhris, Amir ^i,j   Loureiro, José L ^k,l   Gonzalez, Michael A ^m   Mundwiller, Emeline ^a,b,c,d   Deconinck, Tine ^f,h   Wessner, Marc ⁿ   Jornea, Ludmila ^a,b,c   Oteyza, Andrés Caballero ^e   Durr, Alexandra ^a,b,c,o   Martin, Jean Jacques ^h   Schöls, Ludger ^e,p   Mhiri, Chokri ⁱ   Lamari, Foudil ^o   Züchner, Stephan ^m   De Jonghe, Peter ^f,g,h   Kabashi, Edor ^a,b,c   Brice, Alexis ^a,b,c,d,o   Stevanin, Giovanni ^a,b,c,d,o   more..

^a INSTITUT DU CERVEAU ET DE LA MOELLE ÉPINIÈRE   (France)

^b INSERM   (France)

^c CNRS   (France)

^d PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^e UNIVERSITY OF TÜBINGEN   (Germany)

^f UNIVERSITY OF ANTWERP   (Belgium)

^g ANTWERP UNIVERSITY HOSPITAL   (Belgium)

^h UNIVERSITY OF ANTWERP   (Belgium)

ⁱ HABIB BOURGUIBA HOSPITAL   (Tunisia)

^j UNIVERSITY OF SFAX   (Tunisia)

^k UNIVERSITY OF PORTO   (Portugal)

^l Centro Hospitalar Entre Douro e Vouga   (Portugal)

^m UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

ⁿ CENTRE NATIONAL DE SÉQUENÇAGE   (France)

^o ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

^p GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

more..

Author keywords

[No Author keywords available]

Indexed keywords

GBA2 PROTEIN; GLUCOSYLCERAMIDASE; GLUCOSYLCERAMIDE; MESSENGER RNA; MORPHOLINO OLIGONUCLEOTIDE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CATALYSIS; CATARACT; CEREBELLUM ATROPHY; CHROMOSOME 9; CLINICAL ARTICLE; CLINICAL PRACTICE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; EXON; FEMALE; GENE INACTIVATION; GENE SEQUENCE; GENETIC VARIABILITY; HEREDITARY MOTOR SENSORY NEUROPATHY; HUMAN; HUMAN CELL; HYPOGONADISM; LOSS OF FUNCTION MUTATION; MALE; MISSENSE MUTATION; MOTOR NEURON DISEASE; MOUSE; NEUROIMAGING; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; SINGLE NUCLEOTIDE POLYMORPHISM; ZEBRA FISH;

ADOLESCENT; ADULT; AGED; ANIMALS; BETA-GLUCOSIDASE; BRAIN; CHILD; CHILD, PRESCHOOL; FAMILY; FEMALE; HUMANS; INFANT; MALE; MIDDLE AGED; MOTOR NEURONS; MUTATION; NEUROIMAGING; PEDIGREE; SPASTIC PARAPLEGIA, HEREDITARY; YOUNG ADULT; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO;

EID: 84873707921     PISSN: 00029297     EISSN: 15376605     Source Type: Journal    
DOI: 10.1016/j.ajhg.2012.11.021     Document Type: Article

References (38)

1. A.E. Harding Classification of the hereditary ataxias and paraplegias Lancet 1 1983 1151 1155
2. R. Schüle, and L. Schöls Genetics of hereditary spastic paraplegias Semin. Neurol. 31 2011 484 493
3. J. Finsterer, W. Löscher, S. Quasthoff, J. Wanschitz, M. Auer-Grumbach, and G. Stevanin Hereditary spastic paraplegias with autosomal dominant, recessive, X-linked, or maternal trait of inheritance J. Neurol. Sci. 318 2012 1 18
4. A. Boukhris, I. Feki, N. Elleuch, M.I. Miladi, A. Boland-Augé, J. Truchetto, E. Mundwiller, N. Jezequel, D. Zelenika, and C. Mhiri A new locus (SPG46) maps to 9p21.2-q21.12 in a Tunisian family with a complicated autosomal recessive hereditary spastic paraplegia with mental impairment and thin corpus callosum Neurogenetics 11 2010 441 448
5. H. Li, and R. Durbin Fast and accurate short read alignment with Burrows-Wheeler transform Bioinformatics 25 2009 1754 1760
6. M.A. DePristo, E. Banks, R. Poplin, K.V. Garimella, J.R. Maguire, C. Hartl, A.A. Philippakis, G. del Angel, M.A. Rivas, and M. Hanna A framework for variation discovery and genotyping using next-generation DNA sequencing data Nat. Genet. 43 2011 491 498
7. A. McKenna, M. Hanna, E. Banks, A. Sivachenko, K. Cibulskis, A. Kernytsky, K. Garimella, D. Altshuler, S. Gabriel, M. Daly, and M.A. DePristo The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data Genome Res. 20 2010 1297 1303
8. C. Mencarelli, and P. Martinez-Martinez Ceramide function in the brain: when a slight tilt is enough Cell. Mol. Life Sci. 2012
9. H. Matern, R. Gartzen, and S. Matern Beta-glucosidase activity towards a bile acid glucoside in human liver FEBS Lett. 314 1992 183 186
10. H. Matern, H. Heinemann, G. Legler, and S. Matern Purification and characterization of a microsomal bile acid beta-glucosidase from human liver J. Biol. Chem. 272 1997 11261 11267
11. R.G. Boot, M. Verhoek, W. Donker-Koopman, A. Strijland, J. van Marle, H.S. Overkleeft, T. Wennekes, and J.M.F.G. Aerts Identification of the non-lysosomal glucosylceramidase as beta-glucosidase 2 J. Biol. Chem. 282 2007 1305 1312
12. Y. Yildiz, H. Matern, B. Thompson, J.C. Allegood, R.L. Warren, D.M.O. Ramirez, R.E. Hammer, F.K. Hamra, S. Matern, and D.W. Russell Mutation of beta-glucosidase 2 causes glycolipid storage disease and impaired male fertility J. Clin. Invest. 116 2006 2985 2994
13. S. Tsuji, P.V. Choudary, B.M. Martin, B.K. Stubblefield, J.A. Mayor, J.A. Barranger, and E.I. Ginns A mutation in the human glucocerebrosidase gene in neuronopathic Gaucher's disease N. Engl. J. Med. 316 1987 570 575
14. T. Kolter, F. Winau, U.E. Schaible, M. Leippe, and K. Sandhoff Lipid-binding proteins in membrane digestion, antigen presentation, and antimicrobial defense J. Biol. Chem. 280 2005 41125 41128
15. S. van Weely, M. Brandsma, A. Strijland, J.M. Tager, and J.M. Aerts Demonstration of the existence of a second, non-lysosomal glucocerebrosidase that is not deficient in Gaucher disease Biochim. Biophys. Acta 1181 1993 55 62
16. C.M. Walden, R. Sandhoff, C.-C. Chuang, Y. Yildiz, T.D. Butters, R.A. Dwek, F.M. Platt, and A.C. van der Spoel Accumulation of glucosylceramide in murine testis, caused by inhibition of beta-glucosidase 2: implications for spermatogenesis J. Biol. Chem. 282 2007 32655 32664
17. M. Aureli, R. Bassi, N. Loberto, S. Regis, A. Prinetti, V. Chigorno, J.M. Aerts, R.G. Boot, M. Filocamo, and S. Sonnino Cell surface associated glycohydrolases in normal and Gaucher disease fibroblasts J. Inherit. Metab. Dis. 35 2012 1081 1091
18. N. Dekker, T. Voorn-Brouwer, M. Verhoek, T. Wennekes, R.S. Narayan, D. Speijer, C.E.M. Hollak, H.S. Overkleeft, R.G. Boot, and J.M.F.G. Aerts The cytosolic β-glucosidase GBA3 does not influence type 1 Gaucher disease manifestation Blood Cells Mol. Dis. 46 2011 19 26
19. A.C. van der Spoel, M. Jeyakumar, T.D. Butters, H.M. Charlton, H.D. Moore, R.A. Dwek, and F.M. Platt Reversible infertility in male mice after oral administration of alkylated imino sugars: a nonhormonal approach to male contraception Proc. Natl. Acad. Sci. USA 99 2002 17173 17178
20. W. Bone, C.M. Walden, M. Fritsch, U. Voigtmann, E. Leifke, U. Gottwald, S. Boomkamp, F.M. Platt, and A.C. van der Spoel The sensitivity of murine spermiogenesis to miglustat is a quantitative trait: a pharmacogenetic study Reprod. Biol. Endocrinol. 5 2007 1
21. F. Ferreirinha, A. Quattrini, M. Pirozzi, V. Valsecchi, G. Dina, V. Broccoli, A. Auricchio, F. Piemonte, G. Tozzi, and L. Gaeta Axonal degeneration in paraplegin-deficient mice is associated with abnormal mitochondria and impairment of axonal transport J. Clin. Invest. 113 2004 231 242
22. C. Soderblom, J. Stadler, H. Jupille, C. Blackstone, O. Shupliakov, and M.C. Hanna Targeted disruption of the Mast syndrome gene SPG21 in mice impairs hind limb function and alters axon branching in cultured cortical neurons Neurogenetics 11 2010 369 378
23. E. Martin, C. Yanicostas, A. Rastetter, S.M.A. Naini, A. Maouedj, E. Kabashi, S. Rivaud-Péchoux, A. Brice, G. Stevanin, and N. Soussi-Yanicostas Spatacsin and spastizin act in the same pathway required for proper spinal motor neuron axon outgrowth in zebrafish Neurobiol. Dis. 48 2012 299 308
24. M.A. Fox, and J.R. Sanes Synaptotagmin I and II are present in distinct subsets of central synapses J. Comp. Neurol. 503 2007 280 296
25. J.D. Wood, J.A. Landers, M. Bingley, C.J. McDermott, V. Thomas-McArthur, L.J. Gleadall, P.J. Shaw, and V.T. Cunliffe The microtubule-severing protein Spastin is essential for axon outgrowth in the zebrafish embryo Hum. Mol. Genet. 15 2006 2763 2771
26. P. Lin, J. Li, Q. Liu, F. Mao, J. Li, R. Qiu, H. Hu, Y. Song, Y. Yang, and G. Gao A missense mutation in SLC33A1, which encodes the acetyl-CoA transporter, causes autosomal-dominant spastic paraplegia (SPG42) Am. J. Hum. Genet. 83 2008 752 759
27. C. Fassier, J.A. Hutt, S. Scholpp, A. Lumsden, B. Giros, F. Nothias, S. Schneider-Maunoury, C. Houart, and J. Hazan Zebrafish atlastin controls motility and spinal motor axon architecture via inhibition of the BMP pathway Nat. Neurosci. 13 2010 1380 1387
28. L. Southgate, D. Dafou, J. Hoyle, N. Li, E. Kinning, P. Critchley, A.H. Németh, K. Talbot, P.S. Bindu, and S. Sinha Novel SPG11 mutations in Asian kindreds and disruption of spatacsin function in the zebrafish Neurogenetics 11 2010 379 389
29. Y. Song, M. Wang, F. Mao, M. Shao, B. Zhao, Z. Song, C. Shao, and Y. Gong Knockdown of pnpla6 protein results in motor neuron defects in zebrafish Dis. Model Mech. 2012 10.1242/dmm.009688 Published online November 16, 2012
30. H.S. Overkleeft, G.H. Renkema, J. Neele, P. Vianello, I.O. Hung, A. Strijland, A.M. van der Burg, G.J. Koomen, U.K. Pandit, and J.M. Aerts Generation of specific deoxynojirimycin-type inhibitors of the non-lysosomal glucosylceramidase J. Biol. Chem. 273 1998 26522 26527
31. T.M. Cox Gaucher disease: understanding the molecular pathogenesis of sphingolipidoses J. Inherit. Metab. Dis. 24 Suppl 2 2001 106 121 discussion 87-88
32. J.B. Nietupski, J.J. Pacheco, W.-L. Chuang, K. Maratea, L. Li, J. Foley, K.M. Ashe, C.G.F. Cooper, J.M.F.G. Aerts, and D.P. Copeland Iminosugar-based inhibitors of glucosylceramide synthase prolong survival but paradoxically increase brain glucosylceramide levels in Niemann-Pick C mice Mol. Genet. Metab. 105 2012 621 628
33. Y. Sun, H. Ran, B. Liou, B. Quinn, M. Zamzow, W. Zhang, J. Bielawski, K. Kitatani, K.D.R. Setchell, Y.A. Hannun, and G.A. Grabowski Isofagomine in vivo effects in a neuronopathic Gaucher disease mouse PLoS ONE 6 2011 e19037
34. Y. Sun, B. Liou, Y.-H. Xu, B. Quinn, W. Zhang, R. Hamler, K.D.R. Setchell, and G.A. Grabowski Ex vivo and in vivo effects of isofagomine on acid β-glucosidase variants and substrate levels in Gaucher disease J. Biol. Chem. 287 2012 4275 4287
35. G. Stevanin, M. Ruberg, and A. Brice Recent advances in the genetics of spastic paraplegias Curr. Neurol. Neurosci. Rep. 8 2008 198 210
36. S. Edvardson, H. Hama, A. Shaag, J.M. Gomori, I. Berger, D. Soffer, S.H. Korman, I. Taustein, A. Saada, and O. Elpeleg Mutations in the fatty acid 2-hydroxylase gene are associated with leukodystrophy with spastic paraparesis and dystonia Am. J. Hum. Genet. 83 2008 643 648
37. C. Tesson, M. Nawara, M.A. Salih, R. Rossignol, M.S. Zaki, M. Al Balwi, R. Schüle, C. Mignot, E. Obre, and A. Bouhouche Alteration of fatty-acid-metabolizing enzymes affects mitochondrial form and function in hereditary spastic paraplegia Am. J. Hum. Genet. 91 2012 1051 1064
38. R. Schüle, T. Siddique, H.-X. Deng, Y. Yang, S. Donkervoort, M. Hansson, R.E. Madrid, N. Siddique, L. Schöls, and I. Björkhem Marked accumulation of 27-hydroxycholesterol in SPG5 patients with hereditary spastic paresis J. Lipid Res. 51 2010 819 823