Bacterial chitobiase structure provides insight into catalytic mechanism and the basis of Tay–Sachs disease (original) (raw)

References

1. Henrissat, B. & Bairoch, A. New families in the classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem. J. 293, 781–788 (1993).
   Article CAS Google Scholar
2. Davies, G.J. & Henrissat, B. Structures and mechanisms of glycosyl hydrolases. Structure 3, 853–859 (1995).
   Article CAS Google Scholar
3. Chet, I., Barak, Z. & Oppenheim, A.B. Genetic engineering of microorganisms for improved biocontrol activity. in Biotechnology in Plant Disease Control (ed. I. Chet) 211–235 (Wiley Liss, Inc. 1993).
   Google Scholar
4. ZoBell, C.E. & Rittenberg, S.C. The occurence and characteristics of chitinoclastic bacteria in the sea. J. Bacteriol. 35, 275–287 (1937).
   CAS Google Scholar
5. Perrakis, A. et al. Crystal structure of a bacterial chitinase at 2.3 Å resolution. Structure 2, 1169–1180 (1994).
   Article CAS Google Scholar
6. Roey, P.V., Rao, V., Plummer, Jr., T.H. & Tarentino, A.L. Crystal Structure of Endo-β-N-acetylglucosaminidase F1, an α/β-Barrel Enzyme Adapted for a Complex Substrate. Biochem. 33, 13989–13996 (1994).
   Article Google Scholar
7. Rao, V., Guan, C. & Roey, P.V. Crystal structure of endo-β-N-acetylglucosaminidase H at 1.9 Å resolution: active-site geometry and substrate recognition. Structure 3, 449–457 (1995).
   Article CAS Google Scholar
8. Terwisscha van Scheltinga, A.C., Kalk, K.H., Beintema, J.J. & Dijkstra, B.W. Crystal structure of hevamine, a plant defence protein with chitinase and lysozyme activity. Structure 2, 1181–1189 (1994).
   Article CAS Google Scholar
9. Hart, P.J., Pfluger, H.D., Monzingo, A.F., Hollis, T. & Robertus, J.D. The Refined Crystal Structure of the Endochitinase from Hordeum vulgare L. Seeds at 1.8 Å Resolution. J. Mol. Biol. 248, 402–413 (1995).
   Article CAS Google Scholar
10. Oppenheim, A.B. & Chet, I. Cloned chitinases in fungal plant-pathogen control strategies. Trends. Biotech. 10, 392–394 (1992).
    Article Google Scholar
11. Roberts, R.L. & Cabib, E. Serratia marcescens Chitinase: One-Step Purification and Use for the Determination of Chitin. Analyt. Biochem. 127, 402–412 (1982).
    Article CAS Google Scholar
12. Sandhoff, K., Conzelmann, E., Neufeld, E.F., Kaback, M.M. & Suzuki, K. The G M2 ganglosidoses. in The Metabolic Base of Inherited Disease 6th ed. (ed. Scriver, C.R., Beaudet, A.L., Sly, W.S. & Valle, D.) 1807–1842 (McGraw-Hill, New York, 1988).
    Google Scholar
13. Mahuran, D.J. The biochemistry of HEXA and HEXB gene mutations causing GM2 gangliosidosis. Biochim. Biophys. Acta. 1096, 87–94 (1991).
    Article CAS Google Scholar
14. Tews, I., Vincentelli, R. & Vorgias, C.E. _N_-acetylglucosaminidase (chitobiase) from Serratia marcescens: Gene sequence, and protein production and purification in Escherichia coli. Gene 170, 63–67 (1996).
    Article CAS Google Scholar
15. Xu, G.-Y. et al. Solution structure of a cellulose-binding domain from Cellulomonas fimi by nuclear magnetic resonance spectroscopy. Biochem. 34, 6993–7009 (1995).
    Article CAS Google Scholar
16. Baumann, U. Crystal Structure of the 50 kDa Metallo protease from Serratia marcescens. J. Mol. Biol. 242, 244–251 (1994).
    Article CAS Google Scholar
17. Banner, D.W. et al. Structure of chicken muscle triose phosphate isomerase determined crystallographically at 2.5 Å resolution. Nature 255, 609–614 (1975).
    Article CAS Google Scholar
18. De Vos, A.M., Ultsch, M. & Kossiakoff, A.A. Human growth hormone and extracellular domain of its receptor: crystal structure of the complex. Science 255, 306–312 (1992).
    Article CAS Google Scholar
19. Koshland, D.E. Stereochemistry and the mechanism of enzymatic reactions. Biol. Rev. 28, 416–436 (1953).
    Article CAS Google Scholar
20. Paulsen, H. Fortschritte bei der selektiven chemischen Synthese komplexer Oligosaccharide Angew. Chem. Int. Ed.. Engl. 21, 155–173 (1982).
    Article Google Scholar
21. Sinnot, M.L. Stereochemistry and the mechanisms of enzymatic glycosyl transfer. Chem Rev. 90, 1171–1202 (1990).
    Article Google Scholar
22. McCarter, J.D. & Withers, S. Mechanisms of enzymatic glycoside hydrolysis. Curr. Op. Struct. Biol. 4, 885–892 (1994).
    Article CAS Google Scholar
23. Mo, F. & Jensen, L.H. The crystal structure of β-(1→4) linked disaccharide, α-N,N′-diacetylchitobiose monohydrate. Acta Cryst. B34, 1562–1569 (1978).
    Article CAS Google Scholar
24. Lai, E.C.K. & Withers, S.G. Stereochemistry and kinetics of the hydration of 2-acetamido-D-glucal by β-_N_-acetylhexosaminidases. Biochem. 33, 14743–14749 (1994).
    Article CAS Google Scholar
25. Thunissen, A.-M.W.H. et al. Doughnut-shaped structure of a bacterial muraminidase revealed by X-ray crystallography. Nature 367, 750–753 (1994).
    Article Google Scholar
26. Weaver, L.H., Grütter, M.G. & Matthews, B.W. The refined structures of goose lysozyme and its complex with a bound trisaccharide show that the “goose-type” lysozyme lack a catalyticaspartate residue. J. Mol. Biol. 245, 54–68 (1995).
    Article CAS Google Scholar
27. Terwisscha van Scheltinga, A.C. et al. Stereochemistry of chitin hydrolysis by a plant chitinase/lysozyme and X-ray structure of a complex with allosamidin. Evidence for substrate assisted catalysis. Biochem. 34, 15619–115623 (1995).
    Article CAS Google Scholar
28. Lowe, G. & Sheppard, G. Acetamido-group participation in lysozyme catalysis. J. Chem. Soc Chem. Commun. 529–530 (1968).
29. Soto-Gil, R.W. & Zyskind, J.W. N,N′-Diacetylchitobiase of Vibrio harveyi. J. Biol. Chem. 264, 14778–14783 (1989).
    CAS PubMed Google Scholar
30. Somerville, C.C. & Colwell, R.R. Sequence analysis of the b-N-acetylhexosaminidase gene from Vibrio vulnificus: Evidence for a common evolutionary origin of hexosaminidases. Proc. Natl. Acad, Sci. USA 90, 6751–6755 (1993).
    Article CAS Google Scholar
31. Beccari, T., Hoade, J., Orlacchio, A. & Stirling, J.L. Cloning and sequence analysis of a cDNA encoding the α-subunit of mouse β-N-acetylhexosaminidase and comparison with the human enzyme. Biochem. J. 285, 593–596 (1992).
    Article CAS Google Scholar
32. Myerowitz, R., Piekarz, R., Neufeld, E.F., Shows, T.B. & Suzuki, K. human β-hexosaminidase a chain: Coding sequence and homology with the β chain. Proc. Natl. Acad. Sci. USA 82, 7830–7834 (1985).
    Article CAS Google Scholar
33. Bapat, B., Ethier, M., Neote, K., Mahuran, D. & Gravel, R.A. Cloning and sequence analysis of the cDNA encoding the β-subunit of mouse β-hexosaminidase. FEBS Lett. 237, 191–195 (1988).
    Article CAS Google Scholar
34. Muldoon, L.L., Neuwelt, E.A., Pagel, M.A. & Weiss, D.L. Characterization of the molecular defect in feline model for type II GM2 gangliosidoesis (Sandhoff disease). Am. J. Pathol. 144, 1109–1118 (1994).
    CAS PubMed PubMed Central Google Scholar
35. Neote, K. et al. Characterization of the human HEXB gene encoding lysosomal β-hexosaminidase. Genomics 3, 279–286 (1988).
    Article CAS Google Scholar
36. Korneluk, R.G. et al. Isolation of cDNA clones coding for the α-subunit of human β-hexosaminidase. J. Biol. Chem. 261, 8407–8413 (1986).
    CAS PubMed Google Scholar
37. Higgins, D.G., Bleasby, A.J. & Fuchs, R. CLUSTAL V: improved software for multiple sequence alignment. CABIOS 8, 189–191 (1992).
    CAS PubMed Google Scholar
38. Sander, C. & Schneider, R. Database of homogy-derived structures and the structurally meaning of sequence alignment. Proteins 9, 56–68 (1991).
    Article CAS Google Scholar
39. Chothia, C. & Lesk, A.M. The relation between the divergence of sequence and structure in protein. EMBO J. 5, 823–826 (1986).
    Article CAS Google Scholar
40. Rost, B. & Sander, C. Combining evolutionary information and neural networks to predict protein secondary structure. Proteins 19, 55–72 (1994).
    Article CAS Google Scholar
41. Vriend, G. WHAT-IF: A molecular modelling and drug design program. J. Mol. Graph. 8, 52–56 (1990).
    Article CAS Google Scholar
42. Chinea, G., Padron, G., Hooft, R.W.W., Sander, C. & Vriend, G. The use of protein-specific rotamers in model building by homology. Proteins 23, 415–421 (1995).
    Article CAS Google Scholar
43. de Fillippis, V., Sander, C. & Vriend, G. Predicting local structural changes that result from point mutations. Prot. Engng. 7, 1203–1208 (1994).
    Article Google Scholar
44. Kytzia, H.-J. & Sandhoff, K. Evidence for two different active sites on human β-hexosaminidase A. J. Biol. Chem. 260, 7568–7572 (1985).
    CAS PubMed Google Scholar
45. Tanaka, A. et al. GM2-gangliosidosis B1 variant: analysis of β-hexosaminidase a gene abnormalities in seven patients. Am. J. Hum. Genet. 46, 329–339 (1990).
    CAS PubMed PubMed Central Google Scholar
46. Ohno, K. & Suzuki, K. Mutation in GM2 gangliosidosis B1 variant. J. Neurochem. 50, 316–318 (1988).
    Article CAS Google Scholar
47. Triggs-Raine, B.L., Akerman, B.R., Clarke, J.T.R. & Gravel, R.A. Sequence of DNA flanking the exons of the HEXA gene, and identification of mutations in Tay–Sachs Disease. Am. J. Hum. Genet. 49, 1041–1054 (1991).
    CAS PubMed PubMed Central Google Scholar
48. Akli, S., Chelly, J., Lacorte, J.-M., Poenaru, L. & Kahn, A. Seven novel Tay–Sachs mutations detected by chemical mismatch cleavage of PCR-amplified cDNA fragments. Genomics 11, 124–134 (1991).
    Article CAS Google Scholar
49. Fernandes, M. et al. A new Tay–Sachs disease B1 allele in exon 7 in two compound heterozygotes each with a second novel mutation. Hum. Mol. Genet. 1, 759–761 (1992).
    Article CAS Google Scholar
50. Tanaka, A., Punnett, H.H. & Suzuki, K. A new point mutation in the β-hexosaminidase a subunit gene responsible for infantile Tay–Sachs Disease in a non-Jewish Caucasian patient (a Kpn Mutant). Am. J. Hum. Genet. 47, 567–574 (1990).
    Google Scholar
51. Brown, C.A., Neote, K., Leung, A., Gravel, R.A. & Mahuran, D.J. Introduction of the a subunit mutation associated with the B1 variant of Tay–Sachs Disease into the β subunit produces a β-hexosaminidase B without catalytic activity. J. Biol. Chem. 264, 21705–21710 (1989).
    CAS PubMed Google Scholar
52. Brown, C.A. & Mahuran, D.J. Active arginine residues in β-hexosaminidases. J. Biol. Chem. 266, 15855–15862 (1991).
    CAS PubMed Google Scholar
53. Nakano, T. et al. A new point mutation within exon 5 of β-hexosaminidase a gene in a Japanese infant with Tay–Sachs Disease. Ann. Neurol. 27, 465–473 (1990).
    Article CAS Google Scholar
54. Nakano, T., Muscillo, M., Ohno, K., Hoffman, A.J. & Suzuki, K. A point mutatation in the coding sequence of the β-hexosaminidase a gene results in the enzyme protein in an unusual GM2-gangliosidosis variant. J. Neurochem. 51, 984–987 (1988).
    Article CAS Google Scholar
55. Akalin, N. et al. Tay–Sachs Disease in China: two new mutations and a “Macro Polo” allele. Am. J. Hum. Genet. 49, A2246 (1991).
    Google Scholar
56. Ainsworth, P.J. & Coulter-Mackie, M.B. A double mutation in exon 6 of the β-hexosaminidase α subunit in a patient with the B1 variant of Tay–Sachs Disease. Am. J. Hum. Genet. 51, 802–809 (1992).
    CAS PubMed PubMed Central Google Scholar
57. Coulter-Mackie, M.B. Molecular characterization of both alleles in an unusual Tay–Sachs Disease B1 variant. Am. J. Hum. Genet. 54, 1126–1127 (1994).
    CAS PubMed PubMed Central Google Scholar
58. Triggs-Raine, B.L. et al. A pseudodeficiency allele common in non-Jewish Tay–Sachs carriers: implications for carrier screening. Am. J. Hum. Genet. 51, 793–801 (1992).
    CAS PubMed PubMed Central Google Scholar
59. Cao, Z. et al. A second mutation associated with apparent β-hexosaminidase A pseudodeficiency: identification and frequency estimation. Am. J. Hum. Genet. 53, 1198–1205 (1993).
    CAS PubMed PubMed Central Google Scholar
60. Bolhuis, P.A., Ponne, N.J., Bikker, H., Baas, F. & deJong, V.J.M.B. Molecular basis of an adult form of Sandhoff disease: substitution of glutamine for arginine at position 505 of the β-chain of β-hexosaminidase results in a labile enzyme. Biochim. Biophys. Acta. 1182, 142–146 (1993).
    Article CAS Google Scholar
61. Petroulakis, E., Cao, Z., Salo, T., Clarke, J. & Triggs-Raine, B. A Trp474Cys mutation in the alpha-subunit of beta-hexosaminidase causes the subacute encephalopathic form of GM2 gangliosidosis, Type 1. Am. J. Hum. Genet. 55, A2129 (1994).
    Google Scholar
62. Cao, Z., Petroulakis, E., Salo, T. & Triggs-Raine, B. Expression of the HEXA mutations Arg247Trp and Arg249Trp, associated with beta-hexosaminidase A pseudodeficiency. Am. J. Hum. Genet. 55, A1251 (1994).
    Google Scholar
63. Navon, R. & Proia, R.L. The mutations in Ashkenazi Jews with adult GM2 gangliosidosis, the adult form of Tay–Sachs Disease. Science 243, 1471–1474 (1989).
    Article CAS Google Scholar
64. Paw, B.H., Kaback, M.M. & Neufeld, E.F. Molecular basis of adult-onset and chronic GM2 gangliosidosis of Ashkenazi Jewish origin: substitution of serine for glycine at position 269 of the α-subunit of β-hexosaminidase. Proc. Natl. Acad. Sci. USA 86, 2413–2417 (1989).
    Article CAS Google Scholar
65. Brown, C.A. & Mahuran, D.J. β-hexosaminidase Isozymes from cells cotransfected with α and β cDNA constructs: analysis of the α-subunit missense mutation associated with the adult form of Tay–Sachs Disease. Am. J. Hum. Genet. 53, 497–508 (1993).
    CAS PubMed PubMed Central Google Scholar
66. Kless, H., Sitrit, Y., Chet, I. & Oppenheim, A.B. Cloning of the gene coding for chitobiase of Serratia marcescens. Mol. Gen. Genet. 217, 471–473 (1989).
    Article CAS Google Scholar
67. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Meths. Enzymol. 276 (in the press).
68. Furey, W. & Swaminathan, S. PHASES - a program package for the processing and analysis of diffraction data from macromolecules. American Ciystallographic Association Meeting Abstracts 18, 73 (1990).
    Google Scholar
69. Jones, T.A., Zou, J.Y., Cowan, S.W. & Kjeldgaard, M. Improved methods for building models in electron density maps and the location of errors in these models. Acta Crystallogr. A47, 110–119 (1991).
    Article CAS Google Scholar
70. Brünger, A.T. Assessment of phase accuracy by cross validation: the free R value. Methods and application. Acta Crystallogr. D49, 24–36 (1993).
    Google Scholar
71. Konnert, J.H. & Hendrickson, W.A. A restrained-parameter thermal-factor refinement procedure. Acta Crystallogr. A36, 344–350 (1980).
    Article CAS Google Scholar
72. Collaborative Computer Project, Number 4 (CCP4) The CCP4 Suite: Programs for Protein Crystallography. Acta Crystallogr. D50, 760–763 (1994).
73. Lamzin, V.S. & Wilson, K.S. Automated refinement of protein models. Acta Crystallogr. D49, 129–147 (1993).
    CAS Google Scholar
74. Holm, L. & Sander, C. Protein Structure Comparison by Alignment of Distance Matrices. J. Mol. Biol. 233, 123–138 (1993).
    Article CAS Google Scholar
75. van Gunsteren, W.F. & Berendsen, H.J. GROMOS. BIOMOS, Biomolecular Software, University of Groningen, the Netherlands.
76. Kraulis, P. MOLSCRIPT: a program to produce both detailed and schematic plot of protein structures. J. Appl. Crystallogr. 24, 946–950 (1991).
    Article Google Scholar
77. Navon, R. & Proia, R.L. Tay–Sachs Disease in Moroccan Jews: deletion of a phenylalanine in the α-subunit of β-hexosaminidase. Am. J. Hum. Genet. 48, 412–419 (1991).
    CAS PubMed PubMed Central Google Scholar
78. Banerjee, P. et al. Molecular basis of an adult form of β-hexosaminidase B deficiency with motor neuron disease. Biochem. Biophys. Res. Comm. 181, 108–115 (1991).
    Article CAS Google Scholar
79. Mules, E.H., Hayflick, S., Miller, C.S., Reynolds, L.W. & Thomas, G.H. Six novel deleterious and three neutral mutations in the gene encoding the α-subunit of the hexosaminidase A in non-Jewish individuals. Am. J. Hum. Genet. 50, 834–841 (1992).
    CAS PubMed PubMed Central Google Scholar
80. Paw, B.H. et al. Juvenile GM2 gangliosidosis caused by substitution of histidine for arginine at position 499 or 504 of the α-subunit of β-hexosaminidase. J. Biol. Chem. 265, 9452–9457 (1990).
    CAS PubMed Google Scholar
81. Paw, B.H., Wood, L.C. & Neufeld, E.F. A third mutation at the CpG dinucleotide of codon 504 and a silent mutation at codon 506 of the HEXA Gene. Am. J. Hum. Genet. 48, 1139–1146 (1991).
    CAS PubMed PubMed Central Google Scholar
82. Fernandes, M., Boulay, B., Hechtmann, P., Kaplan, F. & Strasberg, P. Five novel HEXA mutations in non-Jewish Tay–Sachs disease (TSD) patients. Am. J. Hum. Genet. 51, A656 (1992).
    Google Scholar

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