Bacterial chitobiase structure provides insight into catalytic mechanism and the basis of Tay-Sachs disease

Nature Structural Biology

Volumn 3, Issue 7, 1996, Pages 638-648

  Tews, Ivo ^a   Perrakis, Anastassis ^a   Oppenheim, Amos ^b   Dauter, Zbigniew ^a   Wilson, Keith S ^a   Vorgias, Constantin E ^c  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b HEBREW UNIVERSITY   (Israel)

^c UNIVERSITY OF ATHENS   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

BETA N ACETYLHEXOSAMINIDASE; CHITINASE;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME CONFORMATION; GENE MUTATION; HUMAN; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; SEQUENCE HOMOLOGY; SERRATIA MARCESCENS; TAY SACHS DISEASE;

ACETYLGLUCOSAMINIDASE; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BETA-N-ACETYLHEXOSAMINIDASE; CATALYSIS; CRYSTALLOGRAPHY, X-RAY; HUMANS; HYDROGEN BONDING; MODELS, STRUCTURAL; MOLECULAR SEQUENCE DATA; POINT MUTATION; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; SANDHOFF DISEASE; SUBSTRATE SPECIFICITY; TAY-SACHS DISEASE;

BACTERIA (MICROORGANISMS); SERRATIA MARCESCENS;

EID: 0029940470     PISSN: 10728368     EISSN: None     Source Type: Journal    
DOI: 10.1038/nsb0796-638     Document Type: Article

References (82)

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).
2. Davies, G.J. & Henrissat, B. Structures and mechanisms of glycosyl hydrolases. Structure 3, 853-859 (1995).
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).
4. ZoBell, CE. & Rittenberg, S.C. The occurence and characteristics of chitinoclastic bacteria in the sea. J. Bacteriol. 35, 275-287 (1937).
5. Perrakis, A. et al. Crystal structure of a bacterial chitinase at 2.3 Å resolution. Structure 2, 1169-1180 (1994).
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. Blochem. 33, 13989-13996 (1994).
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).
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).
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).
10. Oppenheim, A.B. & Chet, I. Cloned chitinases in fungal plant-pathogen control strategies. Trends. Biotech. 10, 392-394 (1992).
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).
12. 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).
13. M2 gangliosidosis. Biochim. Biophys. Acta. 1096, 87-94 (1991).
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).
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).
16. Baumann, U. Crystal Structure of the 50 kDa Metallo protease from Serratia marcescens.J Mol. Biol. 242, 244-251 (1994).
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).
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).
19. Koshland, D.E. Stereochemistry and the mechanism of enzymatic reactions. Biol. Rev. 28, 416-436 (1953).
20. Paulsen, H. Fortschritte bei der selektiven chemischen Synthese komplexer Oligosaccharide Angew. Chem. Int. Ed.. Engl. 21, 155-173 (1982).
21. Sinnot, M.L Stereochemistry and the mechanisms of enzymatic glycosyl transfer. Chem Rev. 90,1171-1202 (1990).
22. McCarter, J.D. & Withers, S. Mechanisms of enzymatic glycoside hydrolysis. Curr. Op. Struct. Biol. 4, 885-892 (1994).
23. Mo, F. & Jensen, L.H. The crystal structure of β-(1→4) linked disaccharide, αN,N'-diacetylchitobiose monohydrate. Acta Cryst. B34, 1562-1569 (1978).
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).
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).
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 catalytic aspartate residue. J. Mol. Biol. 245, 54-68 (1995).
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).
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).
30. Somerviile, 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).
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-acetythexosaminidase and comparison with the human enzyme. Biochem. J. 285, 593-596 (1992).
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).
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).
34. Muldoon, L.L, Neuwelt, E.A., Pagel, M.A. & Weiss, D.L Characterization of the molecular defect in feline model for type II GMZ gangliosidoesis (Sandhoff disease) Am. J. Pathol. 144, 1109-1118 (1994).
35. Neote, K. et al. Characterization of the human HEXB gene encoding lysosomal β-hexosaminidase. Genomics 3, 279-286 (1988).
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).
37. Higgins, D.G., Bleasby, A.J. & Fuchs, R. CLUSTALV: improved software for multiple sequence alignment. CABIOS 8, 189-191 (1992).
38. Sander, C. & Schneider, R. Database of homogy-derived structures and the structurally meaning of sequence alignment. Proteins 9, 56-68 (1991).
39. Chothia C. & Lesk, A.M. The relation between the divergence of sequence and structure in protein. EMBO J. 5, 823-826 (1986).
40. Rost B. & Sander, C. Combining evolutionary information and neural networks to predict protein secondary structure. Proteins 19, 55-72 (1994).
41. Vriend, G. WHAT-IF: A molecular modelling and drug design program. J. Mol. Graph. 8, 52-56 (1990).
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).
43. de Fillippis, V., Sander, C. & Vriend, G. Predicting local structural changes that result from point mutations. Prot. Engng. 7, 1203-1208 (1994).
44. Kytzia, H.-J. & Sandhoff, K. Evidence for two different active sites on human β-hexosaminidase A.J. Biol. Chem. 260, 7568-7572 (1985).
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).
46. Ohno, K. & Suzuki, K. Mutation in GM2 gangliosidosis B1 variant. J. Neurochem. 50, 316-318 (1988).
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).
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).
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).
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).
51. Brown, CA., 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).
52. Brown, C.A. & Mahuran, D.J. Active arginine residues in β-hexosaminidases. J. Biol. Chem. 266, 15855-15862 (1991).
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).
54. M2-gangliosidosis variant. J. Neurochem. 51, 984-987 (1988).
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).
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).
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).
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).
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).
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).
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).
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).
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).
64. M2 gangliosidosis of Ashkenazi Jewish origin: substitution of serine for glycine at position 269 of the α-subunit of β-hexosaminidase. Proc. Natl. Acad. Scid. USA 86, 2413-2417 (1989).
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).
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).
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 Crystallographic Association Meeting Abstracts 18, 73 (1990).
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).
70. Brünger, A.T. Assessment of phase accuracy by cross validation: the free R value. Methods and application. Acta Crystallogr. D49, 24-36 (1993).
71. Konnert, J.H. & Hendrickson, W.A. A restrained-parameter thermal-factor refinement procedure. Acta Crystallogr. A36, 344-350 (1980).
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).
74. Holm, L & Sander, C. Protein Structure Comparison by Alignment of Distance Matrices. J. Mol. Biol. 233, 123-138 (1993).
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).
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).
78. Banerjee, P. etal. Molecular basis of an adult form of β-hexosaminidase B deficiency with motor neuron disease. Biochem. Biophys. Res. Comm. 181, 108-115 (1991).
79. Mules, E.H., Hayflick, S., Miller, CS., Reynolds, LW. & 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).
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).
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).
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).