Molecular characterization of laforin, a dual-specificity protein phosphatase implicated in Lafora disease

Biochimie

Volumn 88, Issue 12, 2006, Pages 1961-1971

  Girard, Jean Marie ^a   Lê, K H Diêp ^a   Lederer, Florence ^a  

^a LABORATOIRE D ENZYMOLOGIE ET BIOCHIMIE STRUCTURALES   (France)

Author keywords

Carbohydrate binding module; Dual specificity phosphatase; Glycogen; Lafora disease; Starch

Indexed keywords

AMYLOSE; BETA CYCLODEXTRIN; CARBOHYDRATE BINDING PROTEIN; CYCLODEXTRIN; GLUTATHIONE TRANSFERASE; LAFORIN; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN; PROTEIN TYROSINE PHOSPHATASE; STARCH;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; ENZYME ACTIVITY; ENZYME ENGINEERING; ENZYME SPECIFICITY; GENE IDENTIFICATION; GENE MUTATION; GENE SEQUENCE; MYOCLONUS EPILEPSY; NUCLEOTIDE SEQUENCE; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING;

AMINO ACID SEQUENCE; BLOTTING, WESTERN; GLYCOGEN; HUMANS; KINETICS; LAFORA DISEASE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN-TYROSINE-PHOSPHATASE; RECOMBINANT FUSION PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SUBSTRATE SPECIFICITY;

EID: 33845445727     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2006.08.002     Document Type: Article

References (53)

1. Lafora G.R., and Glück B. Beitrag zur Histopathologie der myoklonischen Epilepsie. Z. Gesamte Neurol. Psychiat. 6 (1911) 1-14
2. DiMauro S., and Lamperti C. Muscle glycogenoses. Muscle Nerve 24 (2001) 984-999
3. Chan E.M., Andrade D.M., Franceschetti S., and Minassian B. Progressive myoclonus epilepsies: EPM1, EPM2A, EPM2B. Adv. Neurol. 95 (2005) 47-57
4. Cavanagh J.B. Corpora amylacea and the family of polyglucosan diseases. Brain Res. Rev. 29 (1999) 265-295
5. Serratosa J.M., Delgado-Escueta A., Posada I., Shih S., Drury I., Berciano J., Zabala J.A., Antunez M.C., and Sparkes R.S. The gene for progressive myoclonus epilepsy of the Lafora type maps to chromosome 6q. Hum. Mol. Genet. (1995) 1657-1663
6. Sainz J., Minassian B.A., Serratosa J.M., Gee M.N., Sakamoto L.M., Iranmanesh R., Bohlega S., Baumann R.J., Ryan S., Sparkes R.S., and Delgado-Escueta A.V. Lafora progressive myoclonus epilepsy: narrowing the chromosome 6q24 locus by recombinations and homozygosities. Am. J. Hum. Genet. 61 (1997) 1205-1209
7. Serratosa J.M., Gomez-Garre P., Gallardo M.A., Anta B., Beltran-Valero de Bernabé D., Lindhout D., Augustijn P.B., Tassinari C.A., Michelucci R., Malafosse A., Topcu M., Grid D., Dravet C., Berkovic S.F., and de Cordoba S.R. A novel protein tyrosine phosphatase gene is mutated in progressive myoclonus epilepsy of the Lafora type (EPM2). Hum. Mol. Genet. (1999) 345-352
8. Minassian B.A., Lee J.R., Herbrick J.A., Huizenga J., Soder S., Mungall A.J., Dunham I., Gardner R., Fong C.Y., Carpenter S., Jardim L., Satishchandra P., Andrermann E., Snead III O.C., Lopes-Sendes I., Tsui L.C., Delgado-Escueta A.V., Rouleau G.A., and Scherer S.W. Mutations in a gene encoding a novel protein tyrosine phosphatase cause progressive myoclonus epilepsy. Nat. Genet. 20 (1998) 171-174
9. Minassian B.A., Ianzano L., Meloche M., Andermann E., Rouleau G.A., Delgado-Escueta A.V., and Scherer S.W. Mutation spectrum and predicted function of laforin in Lafora's progressive myoclonus epilepsy. Neurology 55 (2000) 341-346
10. Ganesh S., Agarwala K.L., Ueda K., Akagi T., Shoda K., Usui T., Hashikawa T., Osada H., Delgado-Escueta A.V., and Yamakawa K. Laforin, defective in the progressive myoclonus epilepsy of Lafora type, is a dual-specificity phosphatase associated with polyribosomes. Hum. Mol. Genet. 9 (2000) 2251-2261
11. Girard J.M., Lê K.H.D., and Lederer F. Characterization of laforin, a protein phosphatase implicated in the Lafora disease. Protein Sci. 10 Suppl. 1 (2001) 69
12. Wang J., Stuckey J.A., Wishart M.J., and Dixon J.E. A unique carbohydrate binding domain targets the lafora disease phosphatase to glycogen. J. Biol. Chem. 277 (2002) 2377-2380
13. Minassian B.A., Andrade D.M., Ianzano L., Young E.J., Chan E., Ackerley C.A., and Scherer S.W. Laforin is a cell membrane and endoplasmic reticulum-associated protein tyrosine phosphatase. Ann. Neurol. 49 (2001) 271-275
14. Ganesh S., Tsurutani N., Suzuki T., Hoshii Y., Ishihara T., Delgado-Escueta A.V., and Yamakawa K. The carbohydrate-binding domain of Lafora disease protein targets Lafora polyglucosan bodies. Biochem. Biophys. Res. Commun. 313 (2004) 1101-1109
15. Gottlin E.B., Xu X., Epstein D.M., Burke S.P., Eckstein J.W., Ballou D.P., and Dixon J.E. Kinetic analysis of the catalytic domain of human Cdc25B. J. Biol. Chem. 271 (1996) 27445-27449
16. Fernandez-Sánchez M.E., Criado-García O., Heath K.E., García-Fojeda B., Medraño-Fernández I., Gomez-Garre P., Sanz P., Serratosa J.M., and de Cordoba S.R. Laforin, the dual-phosphatase responsible for Lafora disease, interacts with R5 (PTG), a regulatory subunit of protein phosphatase-1 that enhances glycogen accumulation. Hum. Mol. Genet. 12 (2003) 3161-3171
17. Girard J.M., Lê K.H.D., and Lederer F. Laforin, a dual-specificity phosphatase with a starch binding-domain. FEBS J. 272 Suppl. 1 (2005) 295
18. Zhang Z.Y., and VanEtten R.L. Pre-steady-state and steady-state kinetic analysis of the low molecular weight phosphotyrosyl protein phosphatase from bovine heart. J. Biol. Chem. 266 (1991) 1516-1525
19. Dubois M., Gilles K.A., Hamilton J.K., Rebers P.A., and Smith F. Colorimetric method for determination of sugars and related substances. Anal. Chem. 28 (1956) 350-354
20. Kwong C.H., Malech H.L., Rotrosen D., and Leto T.L. Regulation of the human neutrophil NADPH-oxidase of Rho-related G-proteins. Biochemistry 32 (1993) 5711-5717
21. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
22. Coutinho P.M., and Henrissat B. In: Gilbert H.J., Davies G., Henrissat B., and Svensson S. (Eds). Recent Advances in Carbohydrate Bioengineering (1999), The Royal Society of Chemistry, Cambridge 3-12
23. Bouju S., Lignon M.F., Pietu G., Le Cunff M., Leger J.J., Auffray C., and Dechesne C.A. Molecular cloning and functional expression of a novel human gene encoding two 41-43 kDa skeletal muscle internal membrane proteins. Biochem. J. 335 (1998) 549-556
24. Janecek S. A motif of a microbial starch-binding domain found in human genethonin. Bioinformatics 18 (2002) 1534-1537
25. Klein C., and Schulz G.E. Structure of cyclodextrin glycosyltransferase refined at 2.0 Å resolution. J. Mol. Biol. 217 (1991) 737-750
26. Sorimachi K., Jacks A.J., Le Gal-Coeffet M.F., Williamson G., Archer D.B., and Williamson M.P. Solution structure of the granular starch binding domain of glucoamylase from Aspergillus niger by nuclear magnetic resonance spectroscopy. J. Mol. Biol. 259 (1996) 970-987
27. Mikami B., Degano M., Hehre E.J., and Sacchettini J.C. Crystal structures of soybean β-amylase reacted with β-maltose and maltal: active site components and their apparent roles in catalysis. Biochemistry 33 (1994) 7779-7787
28. Knegtel R.M., Strokopytov B., Penninga D., Faber O.G., Rozeboom H.J., Kalk K.H., Dijkhuizen L., and Dijkstra B.W. Crystallographic studies of the interaction of cyclodextrin glycosyltransferase from Bacillus circulans strain 251 with natural substrates and products. J. Biol. Chem. 270 (1995) 29256-29264
29. Sorimachi K., Le Gal-Coeffet M.F., Williamson G., Archer D.B., and Williamson M.P. Solution structure of the granular starch binding domain of Aspergillus niger glucoamylase bound to β-cyclodextrin. Structure 5 (1997) 647-661
30. Barford D., Das A.K., and Egloff M.P. Annu. Rev. Biophys. Biomol. Struct. (1998) 133-164
31. Keyse S.M. Protein phosphatases and the regulation of mitogen-activated protein kinase signalling. Curr. Opin. Cell Biol. 12 (2000) 186-192
32. Farooq A., and Zhou M.M. Structure and regulation of MAPK phosphatases. Cell Signal 16 (2004) 769-779
33. Camps M., Nichols A., and Arkinstall S. Dual specificity phosphatases: a gene family for control of MAP kinase function. FASEB J. 14 (2000) 6-16
34. Bordo D., and Bork P. The rhodanese/Cdc25 phosphatase superfamily - sequence-structure-function relations. EMBO Rep. 3 (2002) 741-746
35. Guan K.L., and Dixon J.E. Eukaryotic proteins expressed in Escherichia coli: an improved thrombin cleavage and purification procedure of fusion proteins with glutathione S-transferase. Anal. Biochem. 192 (1991) 262-267
36. Yuvaniyama J., Denu J.M., Dixon J.E., and Saper M.A. Crystal structure of the dual specificity protein phosphatase VHR. Science 272 (1996) 1328-1331
37. Stuckey J.A., Schubert H.L., Faumann E.B., Zhang Z.Y., Dixon J.E., and Saper M.A. Crystal structure of Yersinia protein tyrosine phosphatase at 2.5 Å and the complex with tungstate. Nature 370 (1994) 571-575
38. Schumacher M.A., Todd J.L., Rice A.E., Tanner K.G., and Denu J.M. Structural basis for the recognition of a bisphosphorylated MAP kinase peptide by human VHR protein phosphatase. Biochemistry 41 (2002) 3009-3017
39. Breslow R. Artificial enzymes and enzyme models. Adv. Enzymol. Relat. Areas. Mol. Biol. 58 (1986) 1-60
40. Zhang Z.Y., Clemens J.C., Schubert H.L., Stuckey J.A., Fischer M.W., Hume D.M., Saper M.A., and Dixon J.E. Expression, purification, and physicochemical characterization of a recombinant Yersinia protein tyrosine phosphatase. J. Biol. Chem. 267 (1992) 23759-23766
41. Zhang Z.Y., Wu L., and Chen L. Transition state and rate-limiting step of the reaction catalyzed by the human dual-specificity phosphatase, VHR. Biochemistry 34 (1995) 16088-16096
42. Wang W., and Roach P.J. Glycogen and related polysaccharides inhibit the laforin dual-specificity protein phosphatase. Biochem. Biophys. Res. Commun. 325 (2004) 726-730
43. Peters G.H., Branner S., Moller K.B., Andersen J.N., and Moller N.P.H. Enzyme kinetic characterization of protein tyrosine phosphatases. Biochimie 85 (2003) 527-534
44. Belshaw N.J., and Williamson G. Interaction of β-cyclodextrin with the granular starch binding domain of glucoamylase. Biochim. Biophys. Acta 1078 (1991) 117-120
45. Bovetto L.J., Backer D.P., Villette J.R., Sicard P.J., and Bouquelet S.J. Cyclomaltodextrin glucanotransferase from Bacillus circulans E 192. I. Purification and characterization of the enzyme. Biotechnol. Appl. Biochem 15 (1992) 48-58
46. Lawson C.L., van Montfort R., Strokopytov B., Rozeboom H.J., Kalk K.H., de Vries G.E., Penninga D., Dijkhuizen L., and Dijkstra B.W. Nucleotide sequence and X-ray structure of cyclodextrin glycosyltransferase from Bacillus circulans strain 251 in a maltose-dependent crystal form. J. Mol. Biol. 236 (1994) 590-600
47. Strokopytov B., Knegtel R.M., Penninga D., Rozeboom H.J., Kalk K.H., Dijkhuizen L., and Dijkstra B.W. Structure of cyclodextrin glycosyltransferase complexed with a maltononaose inhibitor at 2.6 Å resolution. Implications for product specificity. Biochemistry 35 (1996) 4241-4249
48. Giardina T., Gunning A.P., Juge N., Faulds C.B., Furniss C.S., Svensson B., Morris V.J., and Williamson G. Both binding sites of the starch-binding domain of Aspergillus niger glucoamylase are essential for inducing a conformational change in amylose. J. Mol. Biol. 313 (2001) 1149-1159
49. Wu J., Liu J., Thompson I., Oliver C.J., Shenolikar S., and Brautigan D.L. A conserved domain for glycogen binding in protein phosphatase-1 targeting subunits. FEBS Lett. 439 (1998) 185-191
50. Bork P., Dandekar T., Eisenhaber F., and Huynen M. Characterization of targeting domains by sequence analysis: glycogen-binding domains in protein phosphatases. J. Mol. Med. 76 (1998) 77-79
51. Machovic M., Svensson B., MacGregor E.A., and Janecek S. A new clan of CBM families based on bioinformatics of starch-binding domains from families CBM20 and CBM21. FEBS J. 272 (2005) 5497-5513
52. Chan E.M., Ackerley C.A., Lohi H., Ianzano L., Cortez M.A., Shannon P., Scherer S.W., and Minassian B.A. Laforin preferentially binds the neurotoxic starch-like polyglucosans, which form in its absence in progressive myoclonus epilepsy. Hum. Mol. Genet. 13 (2004) 1117-1129
53. Ganesh S., Delgado Escueta A., Suzuki T., Francheschetti S., Riggio C., Avanzini G., Rabinowicz A., Bohlega S., Bailey J., Alonso M.E., Rasmussen A., Thomson A.E., Ochoa A., Prado A.J., Medina M.T., and Yamakawa K. Genotype-phenotype correlations for EPM2A mutations in Lafora's progressive myoclonus epilepsy: exon 1 mutations associate with an early-onset cognitive deficit subphenotype. Hum. Mol. Genet. 11 (2002) 1263-1271