The molecular defect leading to fabry disease: Structure of human α-galactosidase

Journal of Molecular Biology

Volumn 337, Issue 2, 2004, Pages 319-335

  Garman, Scott C ^a   Garboczi, David N ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

EC 3.2.1.22; Fabry disease; Lysosomal storage disease; GAL; GAL, galactosidase; NAGAL; NAGAL, N acetylgalactosaminidase

Indexed keywords

ALPHA GALACTOSIDASE; ASPARTIC ACID; SOMATOMEDIN B RECEPTOR;

ARTICLE; CATALYSIS; CONTROLLED STUDY; ENZYME ANALYSIS; ENZYME STRUCTURE; FABRY DISEASE; HUMAN; HUMAN CELL; LYSOSOME; LYSOSOME STORAGE DISEASE; MISSENSE MUTATION; MOLECULAR BIOLOGY; NONSENSE MUTATION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; X CHROMOSOME LINKED DISORDER; X RAY CRYSTALLOGRAPHY;

EID: 1442299241     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.01.035     Document Type: Article

References (66)

1. Fabry J. Ein Beitrag Zur Kenntnis der Purpura haemorrhagica nodularis (Purpura papulosa hemorrhagica Habrae). Arch. Dermatol. Syph. 43:1898;187.
2. Brady R.O., Gal A.E., Bradley R.M., Martensson E., Warshaw A.L., Laster L. Enzymatic defect in Fabry's disease. Ceramidetrihexosidase deficiency. N. Engl. J. Med. 276:1967;1163-1167.
3. Desnick R.J., Ioannou Y.A., Eng C.M. α-Galactosidase A deficiency: Fabry disease. Scriver C.R., Beaudet A.L., Sly W.S., Valle D. The Metabolic and Molecular Bases of Inherited Disease. 8th edit. 2001;3733-3774 McGraw-Hill, New York.
4. Schiffmann R., Kopp J.B., Austin H.A. III, Sabnis S., Moore D.F., Weibel T., et al. Enzyme replacement therapy in Fabry disease: a randomized controlled trial. JAMA. 285:2001;2743-2749.
5. Eng C.M., Guffon N., Wilcox W.R., Germain D.P., Lee P., Waldek S., et al. Safety and efficacy of recombinant human α-galactosidase A - replacement therapy in Fabry's disease. N. Engl. J. Med. 345:2001;9-16.
6. Beutler E., Grabowski G.A. Gaucher disease. Scriver C.R., Beaudet A.L., Sly W.S., Valle D. The Metabolic and Molecular Bases of Inherited Disease. 8th edit. 2001;McGraw-Hill, New York.
7. Frustaci A., Chimenti C., Ricci R., Natale L., Russo M.A., Pieroni M., et al. Improvement in cardiac function in the cardiac variant of Fabry's disease with galactose-infusion therapy. N. Engl. J. Med. 345:2001;25-32.
8. Park J., Murray G.J., Limaye A., Quirk J.M., Gelderman M.P., Brady R.O., Qasba P. Long-term correction of globotriaosylceramide storage in Fabry mice by recombinant adeno-associated virus-mediated gene transfer. Proc. Natl Acad. Sci. USA. 100:2003;3450-3454.
9. Lee K., Jin X., Zhang K., Copertino L., Andrews L., Baker-Malcolm J., et al. A biochemical and pharmacological comparison of enzyme replacement therapies for the glycolipid storage disorder Fabry disease. Glycobiology. 13:2003;305-313.
10. Zhu A., Leng L., Monahan C., Zhang Z., Hurst R., Lenny L., Goldstein J. Characterization of recombinant α-galactosidase for use in seroconversion from blood group B to O of human erythrocytes. Arch. Biochem. Biophys. 327:1996;324-329.
11. Mayes J.S., Beutler E. α-galactosidase A from human placenta. Stability and subunit size. Biochim. Biophys. Acta. 484:1977;408-416.
12. Dean K.J., Sweeley C.C. Studies on human liver α-galactosidases. I. Purification of α-galactosidase A and its enzymatic properties with glycolipid and oligosaccharide substrates. J. Biol. Chem. 254:1979;9994-10000.
13. Bishop D.F., Desnick R.J. Affinity purification of α-galactosidase A from human spleen, placenta, and plasma with elimination of pyrogen contamination. Properties of the purified splenic enzyme compared to other forms. J. Biol. Chem. 256:1981;1307-1316.
14. Lemansky P., Bishop D.F., Desnick R.J., Hasilik A., von Figura K. Synthesis and processing of α-galactosidase A in human fibroblasts. Evidence for different mutations in Fabry disease. J. Biol. Chem. 262:1987;2062-2065.
15. Hantzopoulos P.A., Calhoun D.H. Expression of the human α-galactosidase A in Escherichia coli K-12. Gene. 57:1987;159-169.
16. Tsuji S., Martin B.M., Kaslow D.C., Migeon B.R., Choudary P.V., Stubbleflied B.K., et al. Signal sequence and DNA-mediated expression of human lysosomal α-galactosidase A. Eur. J. Biochem. 165:1987;275-280.
17. Ioannou Y.A., Bishop D.F., Desnick R.J. Overexpression of human α-galactosidase A results in its intracellular aggregation, crystallization in lysosomes, and selective secretion. J. Cell. Biol. 119:1992;1137-1150.
18. Coppola G., Yan Y., Hantzopoulos P., Segura E., Stroh J.G., Calhoun D.H. Characterization of glycosylated and catalytically active recombinant human α-galactosidase A using a baculovirus vector. Gene. 144:1994;197-203.
19. Chen Y., Jin M., Goodrich L., Smith G., Coppola G., Calhoun D.H. Purification and characterization of human α-galactosidase A expressed in insect cells using a baculovirus vector. Protein Expr. Purif. 20:2000;228-236.
20. Chen Y., Jin M., Egborge T., Coppola G., Andre J., Calhoun D.H. Expression and characterization of glycosylated and catalytically active recombinant human α-galactosidase A produced in Pichia pastoris. Protein Expr. Purif. 20:2000;472-484.
21. Takenaka T., Hendrickson C.S., Tworek D.M., Tudor M., Schiffmann R., Brady R.O., Medin J.A. Enzymatic and functional correction along with long-term enzyme secretion from transduced bone marrow hematopoietic stem/progenitor and stromal cells derived from patients with Fabry disease. Expt. Hematol. 27:1999;1149-1159.
22. Murali R., Ioannou Y.A., Desnick R.J., Burnett R.M. Crystallization and preliminary X-ray analysis of human α-galactosidase A complex. J. Mol. Biol. 239:1994;578-580.
23. Matsuura F., Ohta M., Ioannou Y.A., Desnick R.J. Human α-galactosidase A: characterization of the N-linked oligosaccharides on the intracellular and secreted glycoforms overexpressed by Chinese hamster ovary cells. Glycobiology. 8:1998;329-339.
24. Henrissat B., Davies G. Structural and sequence-based classification of glycoside hydrolases. Curr. Opin. Struct. Biol. 7:1997;637-644.
25. Garman S.C., Hannick L., Zhu A., Garboczi D.N. The 1.9 Å structure of α-N-acetylgalactosaminidase: molecular basis of glycosidase deficiency diseases. Structure. 10:2002;425-434.
26. Fujimoto Z., Kaneko S., Momma M., Kobayashi H., Mizuno H. Crystal structure of rice α-galactosidase complexed with D-galactose. J. Biol. Chem. 278:2003;20313-20318.
27. Koshland D.E. Stereochemistry and the mechanism of enzymatic reactions. Biol. Rev. Cambridge Philos. Soc. 28:1953;416-436.
28. Vasella A., Davies G.J., Bohm M. Glycosidase mechanisms. Curr. Opin. Chem. Biol. 6:2002;619-629.
29. Zechel D.L., Withers S.G. Glycosidase mechanisms: anatomy of a finely tuned catalyst. Acc. Chem. Res. 33:2000;11-18.
30. Garman S.C., Garboczi D.N. Structural basis of Fabry disease. Mol. Genet. Metab. 77:2002;3-11.
31. Miyamura N., Araki E., Matsuda K., Yoshimura R., Furukawa N., Tsuruzoe K., et al. A carboxy-terminal truncation of human α-galactosidase A in a heterozygous female with Fabry disease and modification of the enzymatic activity by the carboxy-terminal domain. Increased, reduced, or absent enzyme activity depending on number of amino acid residues deleted. J. Clin. Invest. 98:1996;1809-1817.
32. Wang A.M., Bishop D.F., Desnick R.J. Human α-N- acetylgalactosaminidase-molecular cloning, nucleotide sequence, and expression of a full-length cDNA. Homology with human α-galactosidase A suggests evolution from a common ancestral gene. J. Biol. Chem. 265:1990;21859-21866.
33. Wang A.M., Ioannou Y.A., Zeidner K.M., Desnick R.J. Murine α-N-acetylgalactosaminidase: isolation and expression of a full-length cDNA and genomic organization: further evidence of an α-galactosidase gene family. Mol. Genet. Metab. 65:1998;165-173.
34. Tsitsanou K.E., Oikonomakos N.G., Zographos S.E., Skamnaki V.T., Gregoriou M., Watson K.A., et al. Effects of commonly used cryoprotectants on glycogen phosphorylase activity and structure. Protein Sci. 8:1999;741-749.
35. Schmidt A., Schlacher A., Steiner W., Schwab H., Kratky C. Structure of the xylanase from Penicillium simplicissimum. Protein Sci. 7:1998;2081-2088.
36. Dean K.J., Sung S.S., Sweeley C.C. The identification of α-galactosidase B from human liver as an α-N- acetylgalactosaminidase. Biochem. Biophys. Res. Commun. 77:1977;1411-1417.
37. Schram A.W., Hamers M.N., Tager J.M. The identity of α- galactosidase B from human liver. Biochim. Biophys. Acta. 482:1977;138-144.
38. Kim W.D., Kobayashi O., Kaneko S., Sakakibara Y., Park G.G., Kusakabe I., et al. α-Galactosidase from cultured rice (Oryza sativa L. var. Nipponbare) cells. Phytochemistry. 61:2002;621-630.
39. Hart D.O., He S., Chany C.J. II, Withers S.G., Sims P.F., Sinnott M.L., Brumer H. III. Identification of Asp-130 as the catalytic nucleophile in the main α-galactosidase from Phanerochaete chrysosporium, a family 27 glycosyl hydrolase. Biochemistry. 39:2000;9826-9836.
40. Ly H.D., Howard S., Shum K., He S., Zhu A., Withers S.G. The synthesis, testing and use of 5-fluoro-α-D-galactosyl fluoride to trap an intermediate on green coffee bean α-galactosidase and identify the catalytic nucleophile. Carbohydr. Res. 329:2000;539-547.
41. McCarter J.D., Withers S.G. Mechanisms of enzymatic glycoside hydrolysis. Curr. Opin. Struct. Biol. 4:1994;885-892.
42. LeDonne N.C. Jr, Fairley J.L., Sweeley C.C. Biosynthesis of α-galactosidase A in cultured Chang liver cells. Arch. Biochem. Biophys. 224:1983;186-195.
43. Ioannou Y.A., Zeidner K.M., Grace M.E., Desnick R.J. Human α-galactosidase A: glycosylation site 3 is essential for enzyme solubility. Biochem J. 332:1998;789-797.
44. Gavel Y., von Heijne G. Sequence differences between glycosylated and non-glycosylated Asn-X-Thr/Ser acceptor sites: implications for protein engineering. Protein Eng. 3:1990;433-442.
45. Ghosh P., Dahms N.M., Kornfeld S. Mannose 6-phosphate receptors: new twists in the tale. Nature Rev. Mol. Cell. Biol. 4:2003;202-212.
46. Davies J.P., Winchester B.G., Malcolm S. Mutation analysis in patients with the typical form of Anderson-Fabry disease. Hum. Mol. Genet. 2:1993;1051-1053.
47. Bishop D.F., Kornreich R., Desnick R.J. Structural organization of the human α-galactosidase A gene: further evidence for the absence of a 3′ untranslated region. Proc. Natl Acad. Sci. USA. 85:1988;3903-3907.
48. Lai L.W., Whitehair O., Wu M.J., O'Meara M., Lien Y.H. Analysis of splice-site mutations of the α-galactosidase A gene in Fabry disease. Clin. Genet. 63:2003;476-482.
49. Ishii S., Suzuki Y., Fan J.Q. Role of Ser-65 in the activity of α-galactosidase A: characterization of a point mutation (S65T) detected in a patient with Fabry disease. Arch. Biochem. Biophys. 377:2000;228-233.
50. Blom D., Speijer D., Linthorst G.E., Donker-Koopman W.G., Strijland A., Aerts J.M. Recombinant enzyme therapy for Fabry disease: absence of editing of human α-galactosidase A mRNA. Am. J. Hum. Genet. 72:2003;23-31.
51. Part A Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Carter C.W. Jr, Sweet R.M. Methods in Enzymology: Macromolecular Crystallography. Methods in Enzymology: Macromolecular Crystallography. vol. 276:1997;307-326 Academic Press, New York.
52. Collaborative Computational Project No. 4. The CCP4 suite: programs for protein crystallography. Acta Crystallog. sect. D. 50:1994;760-763.
53. Brünger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallog. sect. D. 54:1998;905-921.
54. Jones T.A., Zou J.Y., Cowan S.W., Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A. 47:1991;110-119.
55. McKusick V.A. Mendelian Inheritance in Man. A Catalog of Human Genes and Genetic Disorders. 8th edit. 1998;Johns Hopkins University Press, Baltimore.
56. Bairoch A., Apweiler R. The SWISS-PROT protein sequence database and its supplement TrEMBL in 2000. Nucl. Acids Res. 28:2000;45-48.
57. Krawczak M., Cooper D.N. The human gene mutation database. Trends Genet. 13:1997;121-122.
58. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl. Acids Res. 25:1997;3389-3402.
59. Thompson J.D., Higgins D.G., Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl. Acids Res. 22:1994;4673-4680.
60. Bruno W.J., Socci N.D., Halpern A.L. Weighted neighbor joining: a likelihood-based approach to distance-based phylogeny reconstruction. Mol. Biol. Evol. 17:2000;189-197.
61. Felsenstein J. PHYLIP (Phylogeny Inference Package) Version 3.6. 1995;Department of Genetics, University of Washington, Seattle.
62. Needleman S.B., Wunsch C.D. A general method applicable to the search for similarities in the amino acid sequence of two proteins. J. Mol. Biol. 48:1970;443-453.
63. Kleywegt G.J., Read R.J. Not your average density. Structure. 5:1997;1557-1569.
64. Kraulis P.J. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24:1991;946-950.
65. Esnouf R.M. An extensively modified version of MolScript that includes greatly enhanced coloring capabilities. J. Mol. Graph. Model. 15:1997;132-134.
66. Nicholls A., Sharp K.A., Honig B. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins: Struct. Funct. Genet. 11:1991;281-296.