Crystal structures of guinea-pig, goat and bovine α-lactalbumin highlight the enhanced conformational flexibility of regions that are significant for its action in lactose synthase

Structure

Volumn 4, Issue 6, 1996, Pages 691-703

  Pike, Ashley C W ^a,c   Brew, Keith ^b   Acharya, K Ravi ^a  

^a UNIVERSITY OF BATH   (United Kingdom)

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

^c UNIVERSITY OF YORK   (United Kingdom)

Author keywords

Conformational flexibility; Galactosyltransferase; Lactose synthase; X ray crystallography; lactalbumin

Indexed keywords

BOVINAE; CAPRA HIRCUS; CAVIA PORCELLUS; SUS SCROFA;

CALCIUM; GALACTOSYLTRANSFERASE; LACTALBUMIN; LACTOSE SYNTHASE; LYSOZYME; RECOMBINANT PROTEIN;

ANIMAL; ARTICLE; BINDING SITE; CATTLE; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER PROGRAM; GOAT; GUINEA PIG; HUMAN; METABOLISM; MOLECULAR EVOLUTION; PROTEIN CONFORMATION; PROTEIN SECONDARY STRUCTURE; TEMPERATURE; X RAY CRYSTALLOGRAPHY;

ANIMALS; BINDING SITES; CALCIUM; CATTLE; CRYSTALLOGRAPHY, X-RAY; EVOLUTION, MOLECULAR; GALACTOSYLTRANSFERASES; GOATS; GUINEA PIGS; HUMANS; LACTALBUMIN; LACTOSE SYNTHASE; MODELS, MOLECULAR; MURAMIDASE; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; SOFTWARE; TEMPERATURE;

EID: 0030585408     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0969-2126(96)00075-5     Document Type: Article

References (63)

1. Strous, G.J. (1986). Golgi and secreted galactosyltransferase. CRC Crit. Rev. Biochem. 21, 119-151.
2. Khatra, B.S., Herries, D.G. & Brew, K. (1974). Some Kinetic properties of human milk galactosyltransferase. Eur. J. Biochem. 44, 537-560.
3. Bell, J.E., Beyer, T.A. & Hill, R.L. (1976). The kinetic mechanism of bovine milk galactosyltransferase. J. Biol. Chem. 251, 3003-3013.
4. Hill, R.L. & Brew, K. (1975). Lactose synthase. Adv. Enzymol. Rel. Areas Mol. Biol. 43, 411-489.
5. Takase, K. & Ebner, K.E. (1984). Interaction of galctosyltransferase with α-lactalbumin and substrates. Curr. Top. Cell. Reg. 24, 51-62.
6. Brew, K. & Grobler, J.A. (1992). α-Lactalbumin. In Advanced Dairy Chemistry. (Fox, P., ed). vol. 1, pp. 191-229, Elsevier Press, London.
7. Brew, K., Vanaman, T.C. & Hill, R.L. (1967). Comparison of the amino acid sequences of bovine alpha-lactalbumin and hen's egg-white lysozyme. J. Biol. Chem. 242, 3747-3749.
8. Hall, L., Craig, R.K., Edbrooke, M.R. & Campbell, P.N. (1982). Comparison of the nucleotide sequence of cloned human and guineapig pre-alpha-lactalbumin cDNA with that of chick pre-lysozyme cDNA suggests evolution from a common ancestral gene. Nucleic Acids Res. 10, 3503-3515.
9. Acharya, K.R., Stuart, D.I., Walker, N.P.C., Lewis, M. & Phillips, D.C. (1989). Refined structure of baboon α-lactalbumin at 1.7 Å resolution. J. Mol. Biol 208, 99-127.
10. McKenzie, H.A. & White, F.H., Jr. (1991). Lysozyme and α-lactalbumin: structure, function and interrelationships.Adv. Protein Chem. 41, 173-315.
11. Kronman, M.J. (1989). Metal-ion binding and the molecular conformational properties of α-lactalbumin. CRC Crit. Rev. Biochem. Mol. Biol. 24, 565-667.
12. Acharya, K.R., Ren, J., Stuart, D.I., Phillips, D.C. & Fenna, R.E. (1991). Crystal structure of human α-lactalbumin at 1.7 Å resolution. J. Mol. Biol. 221, 571-581.
13. Harata, K. & Muraki, M. (1992). X-ray structural evidence for a local helix-loop transition in α-lactalbumin. J. Biol. Chem. 267, 1419-1421.
14. Grobler, J.A., Rao, R., Pervaiz, S. & Brew, K. (1994). Sequences of two highly divergent canine type c lysozymes: implications for the evolutionary origins of the lysozyme/α-lactalbumin superfamily. Arch. Biochem. Biophys. 313, 360-366.
15. Hiroka, Y., Segawa, Y., Kuwajima, K., Sugai, S. & Murai, N. (1980). α-Lactalbumin: a calcium metalloprotein. Biochem. Biophys. Res. Commun. 93, 1098-1104.
16. 2+ and other divalent metal ions to bovine alpha-lactalbumin. J. Biol. Chem. 256, 8582-8587.
17. Stuart, D.I., Acharya, K.R., Walker, N.P.C., Smith, S.G., Lewis, M. & Phillips, D.C. (1986). α-Lactalbumin possesses a novel calcium binding loop. Nature 324, 84-87.
18. Permyakov, E.A., Kalinichenko, L.P., Morozova, L.A., Yarmolenko, V.V. & Burstein, E.A. (1981). α-Lactalbumin binds magnesium ions: Study by means of intrinsic fluorescence technique. Biochem. Biophys. Res. Commun. 102, 1-7.
19. Strynadka, N.C.J. & James, N.G. (1989). Crystal structures of the helix-loop-helix calcium-binding proteins. Annu. Rev. Biochem. 58, 951-998.
20. Schechter, Y., Patchornik, A. & Burstein, Y. (1974). Selective sulphenylation of tryptophan residues in α-lactalbumin of bovine milk. J. Biol. Chem. 249, 413-419.
21. Prieels, J.P., Bell, J.E., Schindler, M., Castellino, F.J. & Hill, R.L. (1979). Involvement of histidine-32 in the biological activity of α-lactabumin. Biochemistry 18, 1771-1776.
22. Grobler, J.A., Wang, M., Pike, A.C.W. & Brew, K. (1994). Study by mutagenesis of the roles of two aromatic clusters of α-lactalbumin in aspects of its action in the lactose synthase system. J. Biol. Chem. 269, 5106-5114.
23. Richardson, R.H. & Brew, K. (1980). Lactose synthase: an investigation of the interaction site of α-lactalbumin for galactosyltransferase by differential chemical labeling. J. Biol. Chem. 255, 3377-3385.
24. 1NMR assignments and local environments of aromatic residues in bovine, human and guinea-pig variants of α-lactalbumin. Eur. J. Biochem. 210, 699-702.
25. Malinovskii, V.A., Tian, J., Grobler, J.A. & Brew, K. (1996). Functional site in α-lactalbumin encompasses a region corresponding to a subsite in lysozyme and parts of two adjacent flexible substructures. Biochemistry, in press.
26. Blake, C.C.F., Johnson, L.N., Mair, G.A., North, A.C.T., Phillips, D.C. & Sarma, V.R. (1967). Crystallographic studies of the activity of hen egg-white lysozyme. Proc. R. Soc. Lond. [Biol.] 167, 378-388.
27. Pincus, M.R. & Scheraga, H.A. (1981). Prediction of the three-dimensional structure of complexes of lysozyme with cell wall substrates. Biochemistry 20, 3960-3965.
28. Song, H., Inaka, K., Maenaka, K. & Matsushima, M. (1994). Structural changes of active site cleft and different saccharide binding modes in human lysozyme co-crystallised with hexa-N-acetyl-chitohexaose at pH 4.0. J. Mol. Biol. 244, 522-540.
29. Quiocho, F.A. (1986). Carbohydrate-binding proteins: tertiary structures and protein sugar interactions. Annu. Rev. Biochem. 55, 287-315.
30. Johnson, L.N., Cheetham, J., McLaughlin, P.J., Acharya, K.R., Barford, D. & Phillips, D.C. (1988). Protein-oligosaccharide interactions: lysozyme, phosphorylase, amylases. Curr. Top. Microbiol. Immun. 139, 81-134.
31. Lambright, D.G., Lee, T.K. & Wong, S.S. (1985). Association-dissociation modulation of enzymatic activity: case of lactose synthase. Biochemistry 24, 910-914.
32. Powell, J.T. & Brew, K. (1976). A comparison of the interactions of galactosyltransferase with a glycoprotein substrate (ovalbumin) and with α-lactalbumin. J. Biol. Chem. 251, 3653-3663.
33. Berliner, L.J., Davies, M.E., Ebner, K.E., Beyer, T.A. & Bell, J.E. (1984). The lactose synthase acceptor site: a structural map derived from acceptor studies. Mol. Cell. Biochem. 62, 37-42.
34. Qian, M., Haser, R., Buisson, G., Duëe, E. & Payan, F. (1994). The active center of a mammalian α-amylase. Structure of the complex of a pancreatic α-amylase with a carbohydrate inhibitor refined at 2.1 Å resolution. Biochemistry 33, 6284-6289.
35. Ducros, V., et al., & Haser, R. (1995). Crystal structure of the catalytic domain of a bacterial cellulase belonging to family 5. Structure 3, 939-949.
36. Geren, C.R., Magee, S.C. & Ebner, K.E. (1975). Circular dichroism changes in galactosyltransferase upon substrate binding. Biochemistry 14, 1461-1463.
37. Takase, K. & Ebner, K.E. (1981). Interactions of substrates and α-lactalbumin with galactosyltransferase as measured by difference spectroscopy. J. Biol. Chem. 256, 7269-7276.
38. Artymiuk, P. J., Blake, C.C.F., Grace, D.E.P., Oatley, S.J., Phillips, D.C. & Sternberg, M.J.E. (1979). Crystallographic studies of the dynamic properties of lysozyme. Nature 280, 563-568.
39. Blake, C.C.F., Koenig, D.F., Mair, G.A., North, A.C.T., Phillips, D.C. & Sarma, V.R. (1965). Structure of hen egg-white lysozyme. Nature 206, 757-761.
40. Moult, J., et al., & Saya, A. (1976). The structure of triclinic lysozyme at 2.5 Å resolution. J. Mol. Biol. 100, 179-195.
41. Artymiuk, P.J. & Blake, C.C.F. (1981). Refirement of human lysozyme at 1.5 Å resolution. Analysis of non-bonded and hydrogen-bonded interactions. J. Mol. Biol. 152, 737-762.
42. Harata, K. (1993). X-ray structure of monoclinic turkey egg white lysozyme at 1.3Å resolution. Acta Cryst. D 49, 497-504.
43. Smith, L.J., Sutcliffe, M.J., Redfield, C. & Dobson, C.M. (1993). Structure of hen lysozyme in solution. J. Mol. Biol. 229, 930-944.
44. Bradbury, J.H. & Norton, R.S. (1975). Proton-magnetic-resonance spectroscopic study of histidine residues of bovine α-lactalbumin. Eur. J. Biochem. 53, 387-396.
45. Baum, J., Dobson, C.M., Evans, P.A. & Hanley, C. (1989). Characteristaion of a partly folded protein by NMR methods: studies on the molten globule state of guinea-pig α-lactalbumin. Biochemistry 28, 7-13.
46. Macgillivray, R.T.A., Barnes, K. & Brew, K. (1979). The amino acid sequence of goat α-lactalbumin. Arch. Biochem. Biophys. 197, 404-414.
47. Jancarik, J. & Kim, S. (1991). Sparse matrix sampling: a screening method for crystallisation of proteins. J. Appl. Cryst. 24, 409-411.
48. Howard, A., Gilliland, G., Finzel, B., Poulos, T., Ohlendorf, D.H. & Salemme, F.R. (1987). The use of an imaging proportional counter in macromolecular crystallography. J. Appl. Cryst. 20, 383-387.
49. Kabsch, W.J. (1988). Evaluation of single-crystal X-ray diffraction from a position-sensitive detector. J. Appl. Cryst. 21, 916-924.
50. Otwinowski, Z. (1993). Oscillation data reduction program. In Data Collection and Processing, Proceedings of the CCP4 Study Weekend. (Sawyer, L., Isaacs, N. & Bailey, S., eds), pp. 56-62, SERC Daresbury Laboratory, Warrington, UK.
51. Navaza, J. (1994). AMoRe: an automated package for molecular replacement. Acta. Cryst. A 50, 157-163.
52. Collaborative Computational Project, Number 4 (1994). The CCP4 suite: programs for protein crystallography. Acta Cryst. D 50, 760-763.
53. Fitzgreald, P.M.D. (1988). MERLOT, an integrated package of computer programs for determination of crystal structures by molecular replacement. J. Appl. Cryst. 21, 274-28.
54. Brünger, A.T. (1992). X-PLOR: Version 3.1, A System for Crystallography and NMR. Yale University Press, New Haven, CT.
55. Jones, T.A., Zou, J.Y., Cowan, S.W. & Kjeldgaard, M. (1991). Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Cryst. A 47, 110-119.
56. Brünger, A.T. (1992). Free R value: a novel statistical quantity for assesing the accuracy of crystal structures. Nature 355, 472-474.
57. Read, R.J. (1986). Improved Fourier coefficients for maps using phases from partial structures with errors. Acta Cryst. A 42, 140-149.
58. Engh, R.A. & Huber, R. (1991). Accurate bond and angle prameters for X-ray structure refinement. Acta Cryst. A 47, 392-400.
59. Laskowski, R.A., MacArthur, M.W., Moss, D.S. & Thornton, J.M. (1993). PROCHECK: a program to check stereochemical quality of protein structures. J. Appl. Cryst. 26, 283-291.
60. Kraulis, P.J. (1991). MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Cryst. 24, 946-950.
61. Merritt, E.A. & Murphy, M.E.P. (1994). RASTER3D version 2.0: a program for photorealistic molecular graphics. Acta Cryst. D 50, 869-873.
62. Hadfield, A.T., et al., & Johnson, L.N. (1994). Crystal structure of the mutant D52S hen egg-white lysozyme with an oligosaccharide product. J. Mol. Biol. 243, 856-872.
63. Nicholls, A., Sharp, K. & Hoing, B. (1991). Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 11, 281-296.