Molecular divergence of lysozymes and α-lactalbumin

Critical Reviews in Biochemistry and Molecular Biology

Volumn 32, Issue 4, 1997, Pages 255-306

  Qasba, Pradman K ^a   Kumar, Soma ^b  

^a NATIONAL CANCER INSTITUTE   (United States)

^b GEORGETOWN UNIVERSITY   (United States)

Author keywords

Evolution; Galactosyltransferase; Gene organizations; Lactose synthetase; Lysozymes; Molecular divergence; Protein protein interactions; Sequence similarity; lactalbumin

Indexed keywords

ALPHA LACTALBUMIN; LYSOZYME;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ENZYME ANALYSIS; ENZYME MECHANISM; ENZYME STRUCTURE; EVOLUTION; GENE DUPLICATION; HUMAN; LACTATION; MAMMARY GLAND; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SEQUENCE HOMOLOGY;

ANSER SP.; GOES; MAMMALIA; T4 PHAGE;

EID: 0030800608     PISSN: 10409238     EISSN: None     Source Type: Journal    
DOI: 10.3109/10409239709082574     Document Type: Review

References (185)

1. Acharya, K. R., Ren, J., Stuart, D. I., Phillips, D. C., and Fenna, R.E. 1991. Crystal structure of human α-lactalbumin at 1.7 Å resolution. J. Mol. Biol. 22: 571-581.
2. Acharya, K. R., Stuart, D. I., Phillips, D. C., McKenzie, H. A., and Teahan, C. G. 1994. Models of the three-dimensional structures of echidna, horse and pigeon lysozymes: calcium-binding lysozymes and their relationship with α-lactalbumins. J. Prot. Chem. 13: 569-584.
3. Acharya, K. R., Stuart, D. I., Phillips, D. C., and Scheraga, H. 1990. A critical evaluation of the predicted and X-ray structures of α-lactalbumin. J. Prot. Chem. 9: 549-563.
4. Acharya, K. R., Stuart, D. I., Walker, N. P. C., Lewis, M., and Phillips, D. C. 1989. Refined structure of baboon α-lactalbumin at 1.7 Å resolution. J. Mol. Biol. 208: 99-127.
5. Arnheim, N. 1972. Multiple genes for lysozyme. In Lysozymes. pp. 153-161. Osserman, E. F., Canfield, R. E., and Beychok, S., Eds., Academic Press, New York.
6. Aschaffenburg, R., Fenna, R. E., Phillips, D. C., Smith, S. G., Buss, D. H., Jenness, R., and Thompson, M. P. 1979. Crystallography of α-lactalbumin. III. Crystals of baboon milk α-lactalbumin. J. Mol. Biol. 127: 135-137.
7. Bajaj, M. and Blundell, T. 1984. Evolution and the tertiary structure of proteins. Ann. Rev. Biophys. Bioeng. 13: 453-492.
8. Ben-Naim, A., Ting, K. L., and Jernigan, R. L. 1990. Solvent effects on binding thermodynamics of biopolymers. Biopolymers 29: 901-919.
9. Blake, C. C. F., Koenig, D. F., Mair, G. A., North, A. C. T., Phillips, D. C., and Sarma, V. R. 1965. Structure of hen egg-white lysozyme. A three-dimensional Fourier synthesis at 2 Å resolution. Nature (London). 206: 252-761.
10. Boeggeman, E. E., Balaji, P. V., Sethi, N., Masibay, A. A., and Qasba, P. K. 1993. Expression of deletion constructs of bovine 47β-1,4-galactosyltransferase in E. coli: importance of Cys 134 for its activity. Protein Eng. 6: 779-785.
11. Boeggeman, E. E., Balaji, P. V., and Qasba, P. K. 1995. Functional domains of bovine β-1,4-galactosyltransferase. Glycoconjugate J. 12: 865-878.
12. Brew, K. 1970. Lactose synthetase: Evolutionary origin, structure and control. In: Essays in Biochemistry. Vol. 6. pp. 93-118. Campbell, P. N. and Dickens, E., Ed., Academic Press, New York.
13. Brew, K. and Grobbler, J. A. 1992. α-Lactalbumins. In Advanced Dairy Chemistry, pp. 191-229. Vol. 1. Fox, P., ed. Elsevier Press, London.
14. Brew, K., Vanaman, T. C., and Hill, R. L. 1967. Comparison of the amino acid sequence of bovine α-lactalbumin and hen's egg white lysozyme. J. Biol. Chem. 242: 3747-3749.
15. Brew, K., Vanaman, T. C., and Hill, R. L. 1968. The role of α-lactalbumin and the A protein in lactose synthetase: A unique mechanism for the control of a biological reaction. Proc. Natl. Acad. Sci. U.S.A. 59: 491-497.
16. Brodbeck, U. and Ebner, K. E. 1966. Resolution of a soluble lactose synthetase into two protein components and solubilization of microsomal lactose synthetase. J. Biol. Chem. 241: 762-764.
17. Brodbeck, U., Denton, W. L., Tanahashi, N., and Ebner, K. E. 1967. The isolation and identification of the B protein of lactose synthetase as α-lactalbumin. J. Biol. Chem. 242: 1391-1397.
18. Browne, W. J., North, A. C. T., Phillips, D. C., Brew, K., Vanaman, T. C., and Hill, R. L. 1969. A possible three-dimensional structure of bovine α-lactalbumin based on hen's egg-white lysozyme. J. Mol. Biol. 42: 65-89.
19. Canfield, R. E., Collins, J. C., and Sobel, J. H. 1972. Human leukemia lysozyme. In: Lysozymes. pp. 63-70. Osserman, E. F., Canfield, R. E., and Baychock, S., Eds., Academic Press, New York.
20. Canfield, R. E. and McMurry, S. 1967. Purification and characterization of a lysozyme from goose egg white. Biochem. Biophys. Res Comm. 26: 38-42.
21. Cerini, C., Kerjan, P., Astier, M., Gratecos, D., Mirande, M., and Śémériva, M. 1991. A component of the multisynthetase complex is a multifunctional aminoacyl-tRNA synthetase. Embo. J. 10: 4267-4277.
22. Chothia, C. and Lesk, A. M. 1987. The evolution of protein structures. Cold Spring Harbor Symp. Quant. Biol. LII: 399-405.
23. Chothia, C. 1992. One thousand families for the molecular biologist. Nature 357: 543-544.
24. Creighton, T. E. 1993. Evolutionary and genetic origins of protein sequences. In: Proteins, Structure and Molecular Properties, pp. 105-138. W.H. Freeman and Co., New York.
25. Dandekar, A.M. and Qasba, P. K. 1981. Rat α-lactalbumin has a 17-residue-long COOH-terminal hydrophobic extension as judged by sequence analysis of the cDNA clones. Proc. Natl. Acad. Sci. U.S.A. 78: 4853-4857.
26. Dandekar, A. M., Robinson, E. A., Appella, E., and Qasba, P. K. 1982. Complete sequence analysis of cDNA clones encoding rat whey phosphoprotein: homology to a protease inhibitor. Proc. Natl. Acad. Sci. U.S.A. 79: 3987-3991.
27. Dautigny, A., Prager, E. M., Danièle, P.-D., Jollès, J., Pakdel, F., Grinde, B., and Jollès, P. 1991. cDNA and amino acid sequences of rainbow trout (Onchorhyneus mykiss) lysozymes and their implications for the evolution of lysozyme and lactalbumin. J. Mol. Evol. 32: 187-198.
28. Dianoux, A. and Jollés, P. 1967. Étude d'un lysozyme pauvre en cystine at en tryptophan le lysozyme de blanc d'oef d'oie. Biochim. Biophys. Acta. 133: 472-479.
29. Do, K.-Y., Do, S.-I., and Cummings, R. D. 1995. α-Lactalbumin induces bovine milk β1,4- galactosyltransferase to utilize UDP-GalNAc. J. Biol. Chem. 270: 18447-18451.
30. Dobson, C. M., Evans, P. A., and Radford, S. E. 1994. Understanding how proteins fold: the lysozyme story so far. TIBS 19: 31-37.
31. Dobson, D. E., Prager, E. M., and Wilson, A. C. 1984. Stomach lysozymes of ruminants. I. Distribution and catalytic properties. J. Biol. Chem. 259: 11607-11616.
32. Doolittle, R. F. 1985. The geneaology of some recent evolved vertebrate proteins. TIBS 10: 233-237.
33. Doolittle, R., F. 1990. New perspectives on evolution provided by protein sequences. New Perspectives on Evolution. The Wistar Symposium Series 4: 165-173.
34. Ewbank, J. J. and Creighton, T. E. 1993. Structural Characterization of the disulfide folding intermediates of bovine α-lactalbumin. Biochemistry 32: 3694-3707.
35. Fett, R. and Knippers, R. 1991. The primary structure of human glutaminyl-tRNA synthetase. J. Biol. Chem. 266: 1448-1455.
36. Fleming, A. 1922. On a remarkable bacteriolytic element found in tissues and secretions. Proc. Roy. Soc. London B93: 306-317.
37. Fleming, A. 1974. Personal recollections of lysozyme and Fleming. In: Lysozyme. pp. XIII-XVII. Osserman, E. F., Canfield, R. E. and Beychock, S., Eds., Academic Press, New York.
38. Fothergill-Gilmore, L. A. 1986. The evolution of the glycolytic pathway. TIBS 11: 47-51.
39. Freedman, R. B., Hirst, T. R. and Tuite, M. F. 1994. Protein disulfide isomerase: building bridges in protein folding. TIBS 19: 331-336.
40. Gillespie, J. H. 1991. Protein Evolution: Examples of Microadaptations in the Causes of Molecular Evolution, pp. 3-40. Oxford University Press, Oxford.
41. Godovac-Zimmerman, J., Conti, A., and Napolitano, L. 1988. The primary structure of donkey (Equus asinus) lysozyme contains the Ca(II) binding site of α-lactalbumin. Biol. Chem. Hoppe-Seylor. 369: 1109-1115.
42. Godovac-Zimmerman, J., Conti, A., and Napolitano, L. 1990. The complete primary structure of α-lactalbumin isolated from pig (sus scrofa) milk. Biol. Chem. Hoppe-Seyler. 371: 649-653.
43. Goodman, M., Czelusniak, J., Koop, B. F., Tagle, D. A., and Slightom, J. L. 1987. Globins: a case study in molecular phylogeny, In: Evolution of a catalytic function. Cold Spring Harbor Symp. Quant. Biol. LII: 875-890.
44. Grobler, J. A., Rao, K. R., Pervaiz, S. and Brew, K. 1994a. 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.
45. Grobler, J. A., Wang, M., Pike, C. W., and Brew, K. 1994b. 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.
46. Grütter, M. G., Weaver, L. H., and Matthews, B. W. 1983. Goose lysozyme structure: an evolutionary link between hen and bacteriophage lysozymes? Nature (London). 303: 828-830.
47. Hadfield, A. T., Harvey, D. J., Archer, D. B., MacKenzie, D. A., Jeenes, D. J., Radford, S. E., Lowe, G., Dobson, C. M., and Johnson, L. N. 1994. Crystal structure of the mutant D52S hen egg white lysozyme with an oligosaccharide product. J. Mol. Biol. 243: 856-872.
48. 2+-binding site into human lysozyme. Protein Eng. 6: 643-649.
49. Hakansson, A., Zhivotovsky, B., Orrhenius, S., Sabharwal, H., and Svanborg, C. 1995. Apoptosis induced by a human milk protein. Proc Natl. Acad. Sci. U.S.A. 92: 8064-8068.
50. Hall, L. and Campbell, P. N. 1986. α-Lactalbumin and related proteins: a versatile gene family with an interesting parentage. In: Essays in Biochemistry. Vol. 22. pp. 1-26. Marshall, R. D. and Tipton, K. Eds. Academic Press, New York.
51. Hall, L., Emery, C., Davies, S., Parker, D., and Craig, R. K. 1987. Organization and sequence of the human α-lactalbumin gene. Biochem. J. 242: 735-742.
52. Harata, K. and Muraki, M. 1992. X-ray structural evidence for a local helix, loop transition in α-lactalbumin. J. Biol. Chem. 267: 1419-1421.
53. Hartl, D. L. 1991. New Perspectives in the molecular evolution of genes and genomes. In: New Perspectives of Evolution, pp. 123-137. Warren, L. and Koproski, Eds., Wiley-Liss, New York.
54. Hayssen, V. and Blackburn, D. G. 1985. α-Lactalbumin and the origin of lactation. Evolution 39: 1147-1149.
55. Higaki, J. N., Gibson, B. W., and Craik, C. S. 1987. Evolution of catalysis in the serine proteases. In: Evolution of catalytic function. Cold Spring Harbor Symposia on Quant. Biol. LII: 615-621.
56. Hill, R. L. and Brew, K. 1975. Lactose synthetase. In: Advances in Enzymology. 43: 411-490. Interscience Publication, John Wiley, New York.
57. Hiraoka, Y., Segawa, T., Kuwajima, K., Sugai, S., and Murai, N. 1980. α-Lactalbumin: a calcium metalloprotein. Biochem. Biophys. Res. Comm. 95: 1098-1104.
58. Holm, L. and Sander, C. 1996. Mapping the protein universe. Science 273: 595-602.
59. Horwitz, J. 1992. α-Crystallin can function as a molecular chaperone. Proc. Natl. Acad. Sci. U.S.A. 89: 10449-10453.
60. Hyslop, N. E., Jr., Kern, K. C., and Walker, W. A. 1972. Lysozyme in human colostrum and breast milk. In: Lysozymes pp. 449-462, Osserman, E. F., Canfield, R. E., and Beychock, S., Eds., Academic Press, New York.
61. Irwin, D. M., Prager, E. M., and Wilson, A. C. 1992. Evolutionary genetics of ruminant-lysozymes. Animal Genetics 23: 193-202.
62. Irwin, D. M., White, R. T., and Wilson, A. C. 1993. Characterization of the cow stomach lysozyme genes: repetitive DNA and concerted evolution. J. Mol. Evol. 37: 355-356.
63. Irwin, D.M. and Wilson, A.C. 1989. Multiple cDNA sequences and the evolution of bovine stomach lysozyme. J. Biol. Chem. 264: 11387-11393.
64. Irwin, D. M., and Wilson, A. C. 1990. Concerted evolution of ruminant stomach lysozymes. Characterization of lysozyme cDNA clones from sheep and deer. J. Biol. Chem. 265: 4944-4952.
65. Ito, Y., Yamada, H. Nakamura, M., Yoshikawa, A., Ueda, T., and Imoto, T. 1993. The primary structures and properties of non-stomach lysozymes of sheep and cow, and implication for functional divergence of lysozyme. Eur. J. Biochem. 213: 649-658.
66. Jollès, J., Jollès, P., Bowman, B. H., Prager, E. M., Stewart, C.-B., and Wilson, A. C. 1989. Episodic evolution in the stomach lysozymes of ruminants. J. Mol. Evol. 28: 528-535.
67. Jollès, J., Périn, J. P., and Jollès, P. 1977. The ostrich (Struthio camelus) egg white lysozyme. Mol. Cell. Biochem. 17: 39-44.
68. Jollès, J., Prager, E. M., Alnemri, E. S., Jollès, P., Ibrahimi, I. M., and Wilson, A. C. 1990. Amino-acid sequences of stomach and non-stomach lysozymes of ruminants. J. Mol. Evol. 30: 370-382.
69. Jollès, J., Schoentgen, F., Crozier, G., Crozier, L., and Jollès, P. 1979. Insect lysozymes from three species of Lepidoptera: their structural relatedness to the C (chicken) type lysozyme. J. Mol. Evol. 14: 267-271.
70. Jollès, P., Schoentgen, F., Jollès, J., Dobson, D. E., Prager, E. M., and Wilson, A. C. 1984. Stomach lysozymes of ruminants. II. Amino acid sequence of cow lysozyme 2 and immunological comparisons with other lysozymes. J. Biol. Chem. 259: 11617-11625.
71. Jörnvall, H., Höög, J., von Bahr-Lindström, H., and Vallee, B. L. 1987. Mammalian alcohol dehydrogenases of separate classes: intermediates between different enzymes and interclass isoenzymes. Proc. Natl. Acad. Sci. U.S.A. 84: 2580-2584.
72. Jung, A., Sippel, A. E., Grez, M., and Schulz, G. 1980. Exons encode functional and structural units of chicken lysozyme. Proc. Natl. Acad. Sci. U.S.A. 77: 5759-5763.
73. Keese, P. K. and Gibbs, A. 1992. Origin of genes: "Bing bang" or continuous creation. Proc. Natl. Acad. Sci. U.S.A. 89: 9489-9493.
74. Klee, W. A. and Klee, C.B. 1970. The role of α-lactalbumin in lactose synthetase. Biochem. Biophys. Res. Commun. 39: 833-841.
75. Klee, W. A. and Klee, C. B. 1972. The interaction of α-lactalbumin and the A protein of lactose synthetase. J. Biol. Chem. 247: 2336-2344.
76. Koivu, J., Myllylä, R., Halaakoski, T., Pihlajaniemi, T., Tasanen, K., and Kivivikko, K. I. 1987. A single polypeptide acts both as the β subunit of prolyl 4-hydroxylase and as a protein disulfide-isomerase. J. Biol. Chem. 262: 6447-6449.
77. Kornegay, J. R., Schilling, J. W., and Wilson, A. C. 1994. Molecular adaptation of a leaf-eating bird: stomach lysozyme of the hoatzin. Mol. Biol. Evol. 11: 921-928.
78. Kronman, M. J. 1989. Metal ion binding and the molecular conformational properties of α-lactalbumin. Crit. Rev. Biochem. 24: 565-667.
79. Kronman, M. J., Sinha, S., and Brew, K. 1981. Characteristics of the binding of calcium ion and other divalent metal ions to bovine α-lactalburmin. J. Biol. Chem. 256: 8582-8587.
80. Kumagai I., Takeda, S., and Miura, K.-I. 1992. Functional conversion of the homologous proteins α-lactalbumin and lysozyme by exon exchange. Proc. Natl. Acad. Sci. U.S.A. 89: 5887-5891.
81. Kumar, S., Clarke, A. R., Hooper, M. L., Horne, D. S., Law, A. J. R., Leaver, J., Springbett, A., Stevenson, E., and Simons, J. P 1994. Milk composition and lactation of casein-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 91: 6138-6142.
82. Kuroki, R., Kawakita, S., Nakamura, H., and Yutani, K. 1992. Entropic stabilization of a mutant lysozyme induced by calcium binding. Proc. Natl. Acad. Sci. U.S.A. 89: 6803-6807.
83. 2+ binding site in human lysozyme to enhance structural stability. Proc. Natl. Acad, Sci. U.S.A. 86: 6903-6907.
84. Kuroki, R., Weaver, L. H., and Matthews, B. W. 1993. A covalent enzyme-substrate intermediate with saccharide distortion in a mutant T4 lysozyme. Science 262: 2030-2033.
85. 2+ binding on the folding kinetics of α-lactalbumin. J. Mol. Biol. 206: 547-561.
86. Kuziora, M. A., Chalmers, Jr., J. H., Douglas, M. G., Hitzeman, R. A., Mattick, J. S., and Wakil, S. J. 1983. Molecular cloning of fatty acid synthetase genes from Sachharomyces cerevisiae. J. Biol. Chem. 258: 11648-11653.
87. Laird, J. E., Jack, L., Hall, L., Boulton, P., Parker, D., and Craig, R. K. 1988. Structure and expression of the guinea-pig α-lactalbumin gene. Biochem. J. 254: 85-94.
88. Lebioda, L. and Stec, B. 1988. Crystal structure of enolase indicates that enolase and pyruvate kinase evolved from a common ancestor. Nature (London). 333: 683-686.
89. Lee, T. K., Wong, L.-J. C., and Wong, S. S. 1983. Photoaffinity labeling of lactose synthase with a UDP-galactose analog. J. Biol. Chem. 258: 13166-13177.
90. Lonberg, N. and Gilbert, W. 1985. Intron-exon structure of the chicken pyruvate kinase gene. Cell. 40: 81-90.
91. Maenaka, K., Matsushima, M., Song, H., Sunada, F., Watanabe, K., and Kumagai, I. 1995. Dissection of protein-carbohydrate interactions in mutant hen egg white lysozyme complexes and their hydrolytic activity. J. Mol. Biol. 247: 281-293.
92. Malcolm, B. A., Rosenberg, S., Corey, M. J., Allen, J. S., de Baetselier, A., and Kirsch, J. F. 1989. Site-directed mutagenesis of the catalytic residues Asp-52 and Glu-35 of chicken egg white lysozyme. Proc. Natl. Acad. Sci. U.S.A. 86: 133-137.
93. Malinovskii, V., Tian, J., Grobbler, J. A., and 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 35: 9710-9715.
94. Masibay, A. S., Balaji, P. V., Boeggeman, E. E., and Qasba, R. K. 1993. Mutational analysis of the Golgi retention signal of bovine 3-1, 4-galactosyl transferase. J. Biol. Chem. 268: 9908-9916.
95. Mason, D. Y., Jones, M., and Goodnow, C. C. 1992. Development of follicular localization of tolerant B lymphocytes in lysozyme/antilysozyme Ig M/Ig D transgenic mice. Int. Immunol. 4: 163-175.
96. Matthews, B. W., Grütter, M. G., Anderson, W. F., and Remington, S. J. 1981. Common precursor of lysozymes of hen egg white and bacteriophage T4. Nature (London). 290: 334-335.
97. McCarthy, A. D., and Hardie, D. G. 1984. Fatty acid synthetase - an example of protein evolution by gene fusion. TIBS 9: 60-63.
98. McKenzie, H. A. 1996. α-Lactalbumins and lysozymes. In: Lysozymes: Model Enzymes in Biochemistry and Biology, pp. 365-409. Jollés, P., Ed., Birkhauser Verlag, Basel, Switzerland.
99. McKenzie, H.A. and White, F. H., Jr. 1991. Lysozyme and α-lactalbumin: structure, function, and interrelationships. In: Advances in Protein Chemistry, pp. 173-315. Anfinsen, C. B., Edsall, J. T., Richards, F. M., and Edenberg, D. S., Eds., Academic Press, New York.
100. McLachlan, A. D. 1987. Gene duplication and the origin of the repetitive protein structures. Cold Spring Harbor Symp. Quant Biol. LII: 411-420.
101. Means, A. R., Putkey, J. A., and Epstein, P. 1988. Organization and evolution of genes from calmodulin and other calcium binding proteins. In: Calmodulin: Molecular Aspects of Cellular Regulation, pp. 17-33. Cohn, P. and Klee, C. B., Eds., Elsevier, Amsterdam.
102. Meera, G., Ramesh, N., and Brahmachari, S. K. 1989. Zintrons in rat α-lactalbumin gene. FEBS. Lett. 251: 245-249.
103. Messer, M. and Nicholas, K. R. 1991. Biosynthesis of marsupial oligosaccharides: Characterization and developmental changes of two galactosyltransferases in lactating mammary glands of tammar wallaby, Macropus eugenii. Biochim. Biophys. Acta 1077: 79-85.
104. Messier, W. and Stewart, C.-B. 1997. Episodic adaptive evolution of primate lysozymes. Nature 385: 151-154.
105. Morgan, F. J. and Arnheim, N. 1972. Lysozyme of black swan, Cygnus atratus. In: Lysozymes, pp. 81-93. Osserman, E. F., Canfield, R. E., and Beychock, S., Eds., Academic Press, New York.
106. Musci, G. and Berliner, L. (1985). Physiological roles of zinc and calcium binding to α-lactalbumin in lactose biosynthesis. Biochemistry 24: 6945-6948.
107. Nagel, G. M. and Doolittle, R. F. 1991. Evolution and relatedness in two aminoacyl-tRNA synthetase families. Proc. Natl. Acad. Sci. U.S.A. 88: 8121-8125.
108. Neeleman, A. P. and van den Eijnden, D. H. 1996. α-Lactalbumin affects the acceptor specificity of Lymnaea stagnalis albumen gland UDP-GalNAc:GlcNAcβ-R β1 →4-N-acetyl-galactosaminyltransferase: synthesis of GalNAcβ1 Æ 4Glc. Proc. Natl. Acad. Sci. U.S.A. 93: 10111-10116.
109. Neidhart, D. J., Kenyon, G. L., Gerlt, J. A., and Petsko, G. A. 1990. Mandelate racemase and muconate lactonizing enzyme are mechanistically distinct and structurally homologous. Nature 347: 692-694.
110. Newburg, D. S. and Neubauer, S. H. 1995. Carbohydrates in milks. In: Handbook of Milk Composition, pp. 273-349. Jensen, R. G., Ed., Academic Press, New York.
111. Nitta, K. and Sugai, S. 1989. The evolution of lysozyme and α-lactalbumin. Eur. J. Biochem. 182: 111-118.
112. Nitta, K., Tsuge, H., Shimazaki, K., and Sugai, S. 1988. Calcium-binding lysozymes. Biol. Chem. Hoppe-Seyler 369: 671-675.
113. Oftedal, O. T. and Iverson, S. J. 1995. Phylogenetic variation in the gross composition of milks. In: Handbook of Milk Composition, pp. 749-789. Jensen, R. G., Ed., Academic Press, New York.
114. Ohno, S. 1987. Early genes that were oligomeric repeats generated a number of divergent domains on their own. Proc. Natl. Acad. Sci. U.S.A. 84: 6486-6490.
115. Osserman, E. F. 1972. Biological and Clinical studies. Introduction. In: Lysozyme. pp. 303-306. Osserman, E. F., Canfield, R. E., and Beychock, S., Eds., Academic Press, New York.
116. Overington, J., Johnson, M. S., Sali, A., and Blundell, T. L. 1990. Tertiary structural constraints on protein evolutionary diversity templates. Key residues and structure prediction. Proc. R. Soc. Lond. B241: 132-147.
117. Pancholi, V. and Fischetti, V. A. 1993. Glyceraldehyde-3-phosphate dehydrogenase on the surface group A streptococci is also on ADP-ribosylating enzyme. Proc. Natl. Acad. Sci. U.S.A. 90: 8154-8158.
118. (2+)-binding chimera of human lysozyme and bovine α-lactalbumin that can form a molten globule. J. Biol. Chem. 270: 10514-10524.
119. Patel, M. S. and Roche, T. E. 1990. Molecular biology and biochemistry of pyruvate dehydrogenase complexes. FASEB J. 4: 3224-3233.
120. Paulson, J. C. and Colley, K. J. 1989. Glycosyltransferases: structure, localization, and control of cell type-specific glycosylation. J. Biol. Chem. 264: 17615-17618.
121. Pepys, M. B., Hawkins, P. N., Both, D. R., Vigushin, D. M., Tennent, G. A., Soutar, A. K., Totty, M., Nguyen, D., Blake, C. C. F., Terry, C. J., Feest, T. G., Zalin, A. M., and Hsuan, J. J. 1993. Human lysozyme gene mutations cause hereditary systemic amyloidosis. Nature (London) 362: 553-557.
122. 2+ binding to α-lactalbumin. J. Prot. Chem. 13: 277-281.
123. Permyakov, E. A., Shnyrov, V. L., Kalinichenko, L. P., Kuchar, A., Reyzer, I. L., and Berliner, L. J. 1991. Binding of Zn(II) ions to α-lactalburmin. J. Protein Chem. 10: 577-584.
124. Perutz, M. F. 1984. Species adaptation in a protein molecule. In Advances in Protein Chemistry. Vol. 36. pp. 213-244. Anfinsen, C. B., Edsall, J. T., and Richards, F. M., Eds., Academic Press, New York.
125. Peters, C. W., Kruse, U., Pollwein, R., Grzeschik, K.-H. and Sippel, A. E. 1989. The human lysozyme gene. Sequence organization and chromosomal localization. Eur. J. Biochem. 182: 507-516.
126. Phillips, D. C. 1974. Crystallographic studies of lysozyme and its interactions with inhibitors and substrates. In: Lysozyme. pp. 9-30. Osserman, E. F., Canfield, R. E., and Beychock, S., Eds., Academic Press, New York.
127. Piatigorsky, J. and Wistow, G. 1991. The recruitment of crystallins: new functions precede gene duplication. Science 252: 1078-1079.
128. Pike, A. C. W., Brew, K., and Acharya, K. R. 1996. 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 4: 691-703.
129. Post, C. B. and Karplus, M. 1986. Does lysozyme follow the lysozyme pathway? An alternative based on dynamic, structural and stereoelectric considerations, y. Am. Chem. Soc. 108: 1317-1319.
130. Prager, E. M. and Wilson, A. C. 1988. Ancient origin of α-lactalbumin from lysozyme: analysis of DNA and amino acid sequences. J. Mol. Evol. 27: 326-335.
131. Prestrelski, S. J., Byler, D. M., and Thompson, M. P. 1991. Effect of metal ion binding on the secondary structure of bovine α-lactalbumin as examined by infrared spectroscopy. Biochemistry 30: 8797-8804.
132. Qasba, P. K. and Safaya, S. K. 1984. Similarities of the nucleotide sequences of rat α-lactalbumin and chicken lysozyme genes. Nature (London). 308: 377-380.
133. Ramasarma, T. 1994. One protein - many functions. Curr. Sci. India. 67: 24-29.
134. Rao, K. R. and Brew, K. 1989. Calcium regulates folding and disulfide-bond formation in α-lactalbumin. Biochem. Biophys. Res. Comm. 163: 1390-1396.
135. Ren, J., Stuart, D. I., and Acharya, K. R. 1993. α-Lactalbumin possesses a distinct zinc binding site. J. Biol. Chem. 268: 19292-19298.
136. Richardson, R. H. and Brew, K. 1980. lactose synthase. An investigation of the interaction site of α-lactalbumin for galactosyltransferase by differential kinetic labeling. J. Biol. Chem. 255: 3377-3385.
137. Richardson, J. S. and Richardson, D. C. 1989. The de novo design of protein structures. TIBS 14: 304-309.
138. Sax, C. M. and Piatigorsky, J. 1994. Expression of α-crystallin/small heat shock protein/molecular chaperone genes in the lens and other tissues. Advances in Enzymology. Vol. 69. pp. 155-201. Meister, A., Ed., John Wiley & Sons, New York.
139. Schoentgen, F., Jollès, J., and Jollès, P. 1982. Complete aminoacid sequence of ostrich (Struthis camelus) egg white lysozyme, a goose type lysozyme. Eur. J. Biochem. 123: 489-497.
140. Schumacher, G. F. B. 1972. Lysozyme in human genitalia. In: Lysozymes. pp. 427-447. Osserman, E. F., Canfield, R. E., and Beychock, S., Eds. Academic Press, New York.
141. Shaw, D. C., Messer, M., Scrivener, A. M., Nicholas, K. R., and Griffiths. 1993. Isolation, partial characterization, and aminoacid sequence of α-lactalbumin from platypus (Ornithothyneus anatinus) milk. Biochem. Biophys. Acta 1161: 177-186.
142. Shewale, J. G., Sinha, S. K., and Brew, K. 1984. Evolution of α-lactalbumins. The complete amino acid sequence of the α-lactalbumin from a marsupial (Macropus rufogriseus) and corrections to regions of sequences in bovine and goat α-lactalbumins. J. Biol. Chem. 259: 4947-4956.
143. Shih, P. and Kirsch, J. F. 1995. Design and structural analysis of an engineered thermostable chicken lysozyme. Prot. Sci. 4: 2063-2972.
144. Simpson, R. J., Begg, G. S., Dorow, D. S. and Morgan, F. J. 1980. Complete amino acid sequence of goose type lysozyme from egg white of black swan. Biochemistry 19: 1814-1819.
145. Simpson, R. J. and Morgan, F. J. 1983. Complete amino acid sequence of Embden goose (Anser anser) egg white lysozyme. Biochim. Biophys. Acta 744: 349-351.
146. Singh, R. and Green, M. R. 1993. Sequence-specific binding of transfer RNA by glyceraldehyde-3-phosphate dehydrogenase. Science 259: 365-368.
147. Sinha, S. and Brew, K. 1981. A label selection procedure for determining the location of protein-protein interaction sites by cross-linking with bisimidoesters. Application to lactose synthase. J. Biol. Chem. 256: 493-4204.
148. Sinnott, M. J. 1990. Catalytic mechanisms of enzymic glycosyl transfer. Chem. Rev. 90: 1171-1202.
149. Smith, S. G., Lewis, M., Aschffenburg, R., Fenna, R. E., Wilson, I. A., Sundaralingam, M., Stuart, D. I., and Phillips, D. C. 1987. Crystallographic analysis of the three-dimensional structure of baboon α-lactalburmin at low resolution. Ho- mology with lysozyme. Biochem. J. 242: 353-360.
150. Song, H., Inaka, K., Maenaka, K., and Matsushima, M. 1994. Structural changes of active site cleft and different saccharide binding modes in human lysozyme co-crystallized with hexa-N-acetyl chitohexose at pH 4.0. J. Mol. Biol. 244: 522-540.
151. Soulier, S., Mercier, J. C., Vilotte, J. L., Anderson, J., Clark, A. J., and Provot, C. 1989. The bovine and ovine genomes contain multiple sequences homologous to the α-lactalbumin-encoding genes. Gene 83: 331-338.
152. Stacey, A., Schnieke, A., Kerr, M., Scott, A., McKee, C., Cottingham, I., Binus, B., Wilde, C., and Colman, A. 1995. Lactation is disrupted by α-lactalbumin deficiency and can be restored by human α-lactalbumin gene replacement. Proc. Natl. Acad. Sci. U.S.A. 92: 2835-2839
153. Steinhoff, U. M., Senft, B., and Seyfert, H.-M. 1994. Lysozyme-encoding bovine cDNAs from neutrophil granulocytes and mammary gland are derived from a different gene than stomach lysozymes. Gene 143: 271-276.
154. Stewart, C.-B., Schilling, J. W., and Wilson, A. C. 1987. Adaptive evolution in the stomach lysozymes of foregut fermenters. Nature (London) 330: 401-404.
155. Stewart, C.-B. and Wilson, A. C. 1987. Sequence convergence and functional adaptation of stomach lysozymes from foregut fermenters. Cold Spring Harbor Symp. Quant. Biol. LII: 891-899.
156. Stinnakre, M. G., Villotte, J. L., Soulier, S., and Mercier, J. C. 1994. Creation and phenotypic analysis of α-lactalbumin-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 91: 6544-6548.
157. Strynadka, N. C. J. and James, M. N. G. 1991. Lysozyme revisited: crystallographic evidence for distortion of an N-acetylmuramic acid residue bound in site D. J. Mol. Biol. 1991 220: 401-424.
158. Stuart, D. I., Acharya, K. R., Walker, N. P. C., Smith, S. G., Lewis, M., and Phillips, D. C. 1986. α- Lactalbumin possesses a novel calcium binding loop. Nature 324: 84-87.
159. Stumpf, P. 1984. Fatty acid biosynthesis in higher plants. In: Fatty Acid Metabolism and Its Regulation, pp. 155-179. Numa, S., Ed., Elsevier Science Amsterdam.
160. Südhoff, T. C., Goldstein, J. L., Brown, M. S., and Russel, D. W. 1985. The LDL receptor gene. A mosaic of exons shared with different proteins. Science 228: 815-822.
161. Sugai, S. and Ikeguchi, M. 1994. Conformational comparison between α-lactalbumin and lysozyme. Adv. Biophys. 30: 37-84.
162. Swanson, K. W., Irwin, D. M., and Wilson, A. C. 1991. Stomach lysozyme gene of langur monkey: Tests for convergence and positive selection. J. Mol. Evol. 33: 418-425.
163. Takeuchi, K., Irwin, D. M., Gallup, M., Shinbrott, E., Kai, H., Stewart, C.-B. and Basbaum, C. 1993. J. Biol. Chem. 268: 27440-27446.
164. Taylor, D. C., Cripps, A. W., and Clancy, R. L. 1995. A possible role for lysozyme in determining acute exacerbation in chronic bronchitis. Clin. Exp. Immunol. 102: 406-416.
165. Teahan, C. G., McKenzie, H. A., Shaw, D. C., and Griffiths, M. 1991. The isolation and amino acid sequences of echidna (Tachyglossus aculeatus) milk lysozyme I and II. Biochem. Int. 24: 85-95.
166. Tsuge, H., Ago, H., Noma, M., Nitta, K., Sugai, S., and Miyano, M. 1992. Crystallographic studies of a calcium binding lysozyme from equine milk at 2.5 Å resolution. J. Biochem. 111: 141-143.
167. Tsugita, A. 1970. Phage lysozyme and other lytic enzymes. In The Enzymes, Vol. 5, pp. 344-411. Boyer, P., Ed., Academic Press, New York.
168. Vilotte, J.-L., and Soulier, S. 1992. Isolation and characterization of the mouse α-lactalbuminencoding gene: interspecies comparison, tissue- and stage-specific expression. Gene 119: 287-292.
169. Vilotte, J. L., Soulier, S., and Mercier, J.-C. 1992. Sequence of the murine α-lactalbumin-encoding cDNA: interspecies comparison of the coding frame and deduced preprotein. Gene 112: 251-255.
170. Vilotte, J.-L., Soulier, S., Mercier, J.-C., Gaye, P., Hue-Delahaie, D., and Furet, J.-P. 1987. Complete nucleotide sequence of bovine α-lactalbumin gene: comparison with rat counterpart. Biochimie (Paris) 69: 609-620.
171. Vilotte, J. L., Soulier, S., Printz, C., and Mercier, J. C. 1991. Sequences of the goat α-lactalbumin-encoding gene: comparison with the bovine gene and evidence of related sequences in the goat genome. Gene 98: 271-276.
172. Volbeda, A., Lahm, A., Sakiyama, F., and Suck, D. 1991. Crystal structure of Penicilluim citrinum P1 nuclease at 2.8 Å resolution. EMBO J. 10: 1607-1618.
173. Wakil, S. J., 1989. Fatty acid synthase, a proficient multifunctional enzyme. Biochemistry 28: 4523-4530.
174. Wang, M., Scott, W. A., Rao, K. R., Udey, J. Conney, G. E., and Brew, K. 1989. Recombinant bovine α-lactalbumin obtained by limited proteolysis of a fusion protein expressed at high levels in Escherichia coli. J. Biol. Chem. 264: 21116-21121.
175. Warme, P. K., Momany, F. A., Rumball, S. V., Tuttle, R. W., and Scheraga, H. A. 1974. Computation of structures of homologous proteins. α-Lactalbumin from lysozyme. Biochemistry 13: 768-782.
176. Weaver, L. H., Grütter, M. G., and Matthews, B. W. 1995. The refined structures of goose lysozyme and its complex with a bound trisaccharide show that the "goose type" lysozymes lack a catalytic aspartate. J. Mol. Biol. 245: 54-68.
177. White, F. H., Jr., Balkwill, D. L., Meeter, D. A., and Merchant, K. K. 1993. Further studies on the lysozyme-like activity of α-lactalbumin: development of alternative methods of assay. Anal. Biochem. 212: 263-268.
178. Wilson, A. C., Carlson, S. S., and White, T. J. 1977. Biochemical evolution. Annu. Rev. Biochem. 46: 573-639.
179. Wilson, K. P., Malcolm, B. A., and Matthews, B. W. 1992. Structural and thermodynamic analysis of compensating mutations within the core of chicken egg white lysozyme. J. Biol. Chem. 267: 10842-10849.
180. Wistow, G. 1993. Lens crystallins: gene recruitment and evolutionary dynamism. TIBS 18: 301-306.
181. Wylie, D. C. and Vanaman, T. C. 1988. Structure and evolution of the calmodulin family of calcium regulating proteins. In: Calmodulin. pp. 1-15. Cohen, P. and Klee, C. B., Eds., Elsevier Science Publishers, Amsterdam.
182. Yadav, S. and Brew, K. 1990. Identification of UDP-galactose: N-acetylglucosamine 4-galacto- syltranferase involved in UDP-galactose binding by differential labeling. J. Biol. Chem. 265: 14163-14169.
183. Yadav, S. P. and Brew, K. 1991. Structure and function in
184. Yang, D. C. H., Garcia, J. C., Johnson, Y. D., and Wahab, S. 1985. Multienzyme complexes of mammalian aminoacyl-tRNA synthetases. Current Topics in Cellular Regulation 26: 325-335.
185. Zhang, Y., Liang, J.-Y., and Lipscomb, W. N. 1993. Structural similarities between fructose 1,6-biphosphatase and inositol monophosphatase. Biochem. Biophys. Res. Comm. 190: 1080-1083.