Advertisement

α-Lactalbumin

Chapter

Abstract

The whey protein, α-lactalbumin, has a key role in the biosynthesis of lactose and in the formation and secretion of the aqueous phase of milk. Mechanistically, α-lactalbumin interacts with β-1,4-galactosyltransferase-I to modify its specificity so that it can catalyze the transfer of galactose to glucose (lactose synthesis) rather than to glycoconjugates. α-Lactalbumin is a member of the type-c lysozyme superfamily. It has a 3D structure similar to those of the lysozymes that contains a tightly bound stabilizing calcium ion. Complexes of partially folded α-lactalbumin with lipids are cytotoxic to tumor cells but the specificity of this is uncertain.

Keywords

Acceptor Substrate Molten Globule Lactate Mammary Gland Sperm Acrosome Mammary Gland Involution 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

The author wishes to thank the many students and postdoctoral fellows who have previously contributed to studies of α-La and lactose synthase in his laboratory.

References

  1. 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. Comparison with c-type lysozyme. J. Mol. Biol. 208, 99–127.CrossRefGoogle Scholar
  2. Acharya, K.R., Stuart, D.I., Phillips, D.C. and Scheraga, H.A. (1990). A critical evaluation of the predicted and X-ray structures of α-lactalbumin. J. Protein Chem. 9, 549–563.CrossRefGoogle Scholar
  3. Acharya, K.R., Ren, J.S., Stuart, D.I., Phillips, D.C. and Fenna, R.E. (1991). Crystal-structure of human α-latalbumin at 1.7 Å resolution. J. Mol. Biol. 221, 571–581.CrossRefGoogle Scholar
  4. Aramini, J.M., Hiraoki, T., Grace, M.R., Swaddle, T.W., Chiancone, E. and Vogel, H.J. (1996). NMR and stopped-flow studies of metal ion binding to α-lactalbumins. Biochim. Biophys. Acta, 1293, 72–82.CrossRefGoogle Scholar
  5. Berliner, L. and Koga, K. (1987). α-Lactalbumin binding to membranes: evidence for a partially buried protein. Biochemistry, 26, 3006–3009.CrossRefGoogle Scholar
  6. Breton, C., Bettler, E., Joziasse, D.H., Geremia, R.A. and Imberty, A. (1998). Sequence-function relationships of prokaryotic and eukaryotic galactosyltransferases. J. Biochem. 123, 1000–1009.CrossRefGoogle Scholar
  7. Brew, K. (2003). α-Lactalbumin, in Advanced Dairy Chemistry, 3rd edn., Vol. 1, Part A: Proteins, P.F. Fox and P.L.H. McSweeney, eds., New York: Kluwer, pp. 388–418.Google Scholar
  8. Brew, K., Vanaman, T.C. and Hill, R.L. (1967). Comparison of the amino acid sequences of bovine α-lactalbumin and hen’s egg white lysozyme. J. Biol. Chem. 242, 3747–3749.Google Scholar
  9. 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.CrossRefGoogle Scholar
  10. Brinkmann, C.R., Heegaard, C.W., Petersen, T.E., Jensenius, J.C. and Thiel, S. (2011). The toxicity of BAMLET is highly dependent on oleic acid and induces killing in cancer cell lines and non-cancer derived primary cells. FEBS J. 278(11), 1955–1967.CrossRefGoogle Scholar
  11. 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.Google Scholar
  12. 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 that of hen’s egg-white lysozyme. J. Mol. Biol. 42, 65–86.CrossRefGoogle Scholar
  13. Calderone, V., Giuffrida, M.G., Viterbo, D., Napolitano, L., Fortunate, D., Conti, A. and Acharya, K.R. (1996). Amino acid sequence and crystal structure of buffalo α-lactalbumin. FEBS Lett. 394, 91–95.CrossRefGoogle Scholar
  14. Campbell, J.A., Davies, G.J., Bulone, V. and Henrissat, B. (1997). A classification of nucleotide-diphospho-sugar glycosyltransferases based on amino acid sequence similarities. Biochem. J. 326, 929–939.Google Scholar
  15. Capuco, A.V. and Akers, R.M. (2009). The origin and evolution of lactation. J. Biol. 8, 37.CrossRefGoogle Scholar
  16. Chandra, N., Brew, K. and Acharya, K.R. (1998). Structural evidence for the presence of a secondary calcium binding site in human α-lactalbumin. Biochemistry, 37, 4767–4772.CrossRefGoogle Scholar
  17. Chiu, W.W., Erikson, E.K., Sole, C.A., Shelling, A.N. and Chamley, L.W. (2004). SPRASA, a novel sperm protein involved in immune-mediated infertility. Hum. Reprod. 19, 243–249.CrossRefGoogle Scholar
  18. Chrysina, E.D., Brew, K. and Acharya, K.R. (2000). Crystal structures of apo- and holo-bovine α-lactalbumin at 2.2 Å resolution reveal an effect or Ca2+ on inter-lobe interactions. J. Biol. Chem. 275, 37021–37029.CrossRefGoogle Scholar
  19. Coutinho, P.M., Deleury, E., Davies, G.J. and Henrissat, B. (2003). An evolving hierarchical family classification for glycosyltransferases. J. Mol. Biol. 328, 307–317.CrossRefGoogle Scholar
  20. Davies, M.S., West, L.F., Davis, M.B., Povey, S. and Craig, R.K. (1987). The gene for human α-lactalbumin is assigned to chromosome 12q13. Ann. Hum. Genet. 51, 183–188.CrossRefGoogle Scholar
  21. Dereeper, A., Guignon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F., Dufayard, J.F., Guindon, S., Lefort, V., Lescot, M., Claverie, J.M. and Gascuel, O. (2008). Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 36, W465–W469.CrossRefGoogle Scholar
  22. Forge, V., Wijesinha, R.T., Balbach, J., Brew, K., Robinson, C.V., Redfield, C. and Dobson, C.M. (1999). Rapid collapse and slow structural reorganization during the refolding of bovine α-lactalbumin. J. Mol. Biol. 288, 673–688.CrossRefGoogle Scholar
  23. Godovac-Zimmermann, 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. 369, 1109–1115.Google Scholar
  24. Grobler, J., Rao, K.R., Pervaiz, S. and Brew, K. (1994). Sequences of two highly divergent canine type c lysozymes; implications for evolutionary interrelationships in the lysozyme/α-lactalbumin superfamily. Arch. Biochem. Biophys. 313, 360–366.CrossRefGoogle Scholar
  25. Grunclova, L., Fouquier, H., Hypsa, V. and Kopacek, P. (2003). Lysozyme from the gut of the soft tick Ornithodoros moubata: the sequence, phylogeny and post-feeding regulation. Dev. Comp. Immunol. 27, 651–660.CrossRefGoogle Scholar
  26. Gustafsson, L., Leijonhufvud, I., Aronsson, A., Mossberg, A.K. and Svanborg, C. (2004). Treatment of skin papillomas with topical alpha-lactalbumin-oleic acid. N. Engl. J. Med. 350, 2663–2672.CrossRefGoogle Scholar
  27. Hakansson, A., Zhivotovsky, B., Orrenius, S., Sabharwal, H. and Svanborg, C. (1995). Apoptosis induced by a human milk protein. Proc. Natl. Acad. Sci. U.S.A. 92, 8064–8068.CrossRefGoogle Scholar
  28. Hakansson, A., Andreasson, J., Zhivotovsky, B., Karpman, D., Orrenius, S. and Svanborg, C. (1999). Multimeric α-lactalbumin from human milk induces apoptosis through a direct effect on cell nuclei. Exp. Cell Res. 246, 451–460.CrossRefGoogle Scholar
  29. Hall, L., Emery, D.C., Davies, M.S., Parker, D. and Craig, R.F. (1987). Organization and sequence of the human α-lactalbumin gene. Biochem. J. 242, 735–742.Google Scholar
  30. Harata, K. and Muraki, M. (1992). X-Ray structural evidence for a local helix-loop transition in α-lactalbmin. J. Biol. Chem. 267, 1419–1421.Google Scholar
  31. Hiroaka, Y., Segawa, T., Kuwajima, K., Sugai, S. and Murai, N. (1980). α-Lactalbumin: a calcium metallo-protein. Biochem. Biophys. Res. Commun. 93, 1098–1104.CrossRefGoogle Scholar
  32. Irwin, D.M., Biegel, J.M. and Stewart, C.-B. (2011). Evolution of the mammalian lysozyme gene family. BMC Evol. Biol. 11, 166.CrossRefGoogle Scholar
  33. Kronman, M.J., Sinha, S.K. and Brew, K. (1981) Characteristics of the Binding of Ca2+ and Other Divalent Metal Ions to Bovine α-Lactalbumin. J. Biol. Chem. 256, 8582–­8587.CrossRefGoogle Scholar
  34. Kohler, C., Hakansson, A., Svanborg, C., Orrenius, S. and Zhivotovsky, B. (1999). Protease activation in apoptosis induced by MAL. Exp. Cell Res. 249, 260–268.CrossRefGoogle Scholar
  35. Kuwajima, K. (1989). The molten globule state as a clue for understanding the folding and cooperativity of globular-protein structure. Proteins, 6, 87–103.CrossRefGoogle Scholar
  36. Kuwajima, K. (1996). The molten globule state of α-lactalbumin. FASEB J. 10, 102–109.Google Scholar
  37. Kuwajima, K., Mitani, M. and Sugai, S. (1989). Characterization of the critical state in protein folding-effects of guanidine hydrochloride and specific Ca2+ binding on the folding kinetics of α-lactalbumin. J. Mol. Biol. 206, 547–561.CrossRefGoogle Scholar
  38. Li, B., Calvo, E., Marinotti, O., James, A.A. and Paskewitz, S.M. (2005). Characterization of the c-type lysozyme gene family in Anopheles gambiae. Gene 360, 131–139.CrossRefGoogle Scholar
  39. Lindahl, L. and Vogel, H.J. (1984). Metal-ion dependent hydrophobic-interaction chromatography of α-lactalbumin. Anal. Biochem. 140, 394–402.CrossRefGoogle Scholar
  40. Liskova, K., Kelly, A.L., O’Brien, N. and Brodkorb, A. (2010). Effect of denaturation of alpha-lactalbumin on the formation of BAMLET (bovine alpha-lactalbumin made lethal to tumor cells). J. Agric. Food Chem. 58, 4421–4427.CrossRefGoogle Scholar
  41. Lo, N.W., Shaper, J.H., Pevsner, J. and Shaper, N.L. (1998). The expanding β4-galactosyltransferase gene family: messages from the databanks. Glycobiology 8, 517–526.CrossRefGoogle Scholar
  42. Malinovskii, V.A., Tian, J., Grobler, 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.CrossRefGoogle Scholar
  43. Mandal, A., Klotz, K.L., Shetty, J., Jayes, F.L., Wolkowicz, M.J., Bolling, L.C., Coonrod, S.A., Black, M.B., Diekman, A.B., Haystead, T.A., Flickinger, C.J. and Herr, J.C. (2003). SLLP1, a unique, intra-acrosomal, non-bacteriolytic, c lysozyme-like protein of human spermatozoa. Biol. Reprod. 68, 1525–1537.CrossRefGoogle Scholar
  44. Masibay, A.S., Balaji, P.V., Boeggeman, E.E. and Qasba, P.K. (1993). Mutational analysis of the Golgi retention signal of bovine beta-1,4-galactosyltransferase. J. Biol. Chem. 268, 9908–9916.Google Scholar
  45. Messer, M., Griffiths, M., Rismiller, P.D. and Shaw, B.C. (1997). Lactose synthesis in a monotreme, the echidna (Tachyglossus aculeatus): isolation and amino acid sequence of echidna α-lactalbumin. Comp. Biochem. Physiol. B 118, 403–410.Google Scholar
  46. Mok, K.H., Pettersson, J., Orrenius, S. and Svanborg, C. (2007). HAMLET, protein folding, and tumor cell death. Biochem. Biophys. Res. Commun. 354, 1–7.CrossRefGoogle Scholar
  47. Mossberg, A.K., Wullt, B., Gustafsson, L., Månsson, W., Ljunggren, E. and Svanborg, C. (2007). Bladder cancers respond to intravesical instillation of HAMLET (human alpha-lactalbumin made lethal to tumor cells). Int. J. Cancer, 121, 1352–1359.CrossRefGoogle Scholar
  48. Mossberg, A.K., Mok, K.H., Morozova-Roche, L.A. and Svanborg, C. (2010). Structure and function of human alpha-lactalbumin made lethal to tumor cells (HAMLET)-type complexes. FEBS J. 277, 4614–4625.CrossRefGoogle Scholar
  49. Musci, G. and Berliner, L.J. (1985). Physiological roles of zinc and calcium binding to α-lactalbumin in lactose biosynthesis. Biochemistry 24, 6945–6948.CrossRefGoogle Scholar
  50. Narimatsu, H., Sinha, S., Brew, K., Okayama, H. and Qasba, P.K. (1986). Cloning and sequencing of cDNA of bovine N-acetylglucosamine (β 1–4) galactosyltransferase. Proc. Natl. Acad. Sci. U.S.A. 83, 4720–4724.CrossRefGoogle Scholar
  51. Nielsen, S.B., Wilhelm, K., Vad, B., Schleucher, J., Morozova-Roche, L.A. and Otzen, D. (2010). The interaction of equine lysozyme:oleic acid complexes with lipid membranes suggests a cargo off-loading mechanism. J. Mol. Biol. 398, 351–361.CrossRefGoogle Scholar
  52. Nitta, K. and Sugai, S. (1989). The evolution of lysozyme and α-lactalbumin. Eur. J. Biochem. 182, 111–118.CrossRefGoogle Scholar
  53. Oftedal, O.T. (2002). The mammary gland and its origin during synapsid evolution. J. Mammary Gland Biol. Neoplasia, 7, 225–252.CrossRefGoogle Scholar
  54. Pan, L., Yue, F., Miao, J., Zhang, L. and Li, J. (2010). Molecular cloning and characterization of a novel c-type lysozyme gene in swimming crab Portunus trituberculatus. Fish Shellfish Immunol. 29, 286–292.CrossRefGoogle Scholar
  55. Peters, C.W.B., Kruse, U., Pollwein, R., Grzeschik, K.-H. and Sippel, A.E. (1989). The human lysozyme gene: sequence organization and chromosomal localization. Cytogenet. Cell Genet. 51, 1059.Google Scholar
  56. Permyakov SE, Knyazeva EL, Leonteva MV, Fadeev RS, Chekanov AV, Zhadan AP, Håkansson AP, Akatov VS, Permyakov EA (2011). A novel method for preparation of HAMLET-­like protein complexes. Biochemistry, 93, 1495–1501.CrossRefGoogle Scholar
  57. Pettersen, E.F., Goddard, T.D., Huang, C.C., Couch, G.S., Greenblatt, D.M., Meng, E.C. and Ferrin, T.E. (2004). UCSF Chimera–a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612.CrossRefGoogle Scholar
  58. Pike, A.C.W., Acharya, K.R. and Brew, K. (1996). Crystal structures of guinea-pig, goat and bovine α-lactalbumins highlight the enhanced conformational flexibility of regions that are significant for its action in lactose synthase. Structure, 4, 691–703.CrossRefGoogle Scholar
  59. Powell, J.T. and Brew, K. (1976). A comparison of the interactions of galactosyl-transferase with a glycoprotein substrate (ovalbumin) and with α-lactalbumin. J. Biol. Chem. 251, 3653–3663.Google Scholar
  60. 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.CrossRefGoogle Scholar
  61. Qasba, P.K. and Safaya, S.K. (1984). Similarities in the nucleotide sequences of rat α-lactalbumin and chicken lysozyme genes. Nature 308, 377–380.CrossRefGoogle Scholar
  62. Qasba, P.K., Ramakrishnan, B. and Boeggeman, E. (2008). Structure and function of β-1,4 galactosyltransferase. Curr. Drug Targets 9, 292–309.CrossRefGoogle Scholar
  63. Ramakrishnan, B. and Qasba, P.K. (2001). Crystal structure of lactose synthase reveals a large conformational change in its catalytic component, the β-1,4-galactosyltransferase-I.J. Mol. Biol. 310, 205–218.CrossRefGoogle Scholar
  64. Ramakrishnan, B., Boeggeman, E., Ramasamy, V. and Qasba, P.K. (2004). Structure and catalytic cycle of beta-1,4-galactosyltransferase. Curr. Opin. Struct. Biol. 14, 593–600.CrossRefGoogle Scholar
  65. Ramakrishnan, B., Ramasamy, V. and Qasba, P.K. (2006). Structural snapshots of beta-1,4-galactosyltransferase-I along the kinetic pathway. J. Mol. Biol. 357, 619–633.CrossRefGoogle Scholar
  66. Rao, K.R. and Brew, K. (1989). Calcium regulates folding and disulfide-bond formation in α-lactalbumin. Biochem. Biophys. Res. Commun. 163, 1390–1396.CrossRefGoogle Scholar
  67. Reich, C.M. and Arnould, J.P.Y. (2007). Evolution of Pinnipedia lactation strategies: a potential role for α-lactalbumin. Biol. Lett. 3, 546–549.CrossRefGoogle Scholar
  68. Ren, J., Stuart, D.I. and Acharya, K.R. (1993). α-Lactalbumin possesses a distinct zinc binding site. J. Biol. Chem. 268, 19292–19298.Google Scholar
  69. Rodriguez, R., Menendez-Arias, L., Gonzalez de Buitrago, G. and Gavilanes, J.G. (1985). Amino acid sequence of pigeon egg-white lysozyme. Biochem. Int. 11, 841–843.Google Scholar
  70. Rösner, H.I. and Redfield, C. (2009). The human alpha-lactalbumin molten globule: comparison of structural preferences at pH 2 and pH 7. J. Mol. Biol. 394, 351–362.CrossRefGoogle Scholar
  71. Rychel, A.L., Reeder, T.W. and Berta, A. (2004). Phylogeny of mysticete whales based on mitochondrial and nuclear data. Mol. Phylogenet. Evol. 32, 892–901.CrossRefGoogle Scholar
  72. Shaper, N.L., Shaper, J.H., Meuth, J.L., Fox, J.L., Chang, H., Kirsch, I.R. and Hollis, G.F. (1986). Bovine galactosyltransferase: identification of a clone by direct immunological screening of a cDNA expression library. Proc. Natl. Acad. Sci. U.S.A. 83, 1573–1577.CrossRefGoogle Scholar
  73. Sharp, J.A., Lefèvre, C. and Nicholas, K.R. (2008). Lack of functional α-lactalbumin prevents involution in Cape fur seals and identifies the protein as an apoptotic milk factor in mammary gland involution. BMC Biol. 6, 48.CrossRefGoogle Scholar
  74. Shaw, D.C., Messer, M., Scrivener, A.M., Nicholas, K.R. and Griffiths, M. (1993). Isolation, partial characterisation, and amino acid sequence of α-lactalbumin from platypus (Ornithorhynchus anatinus) milk. Biochim. Biophys. Acta, 1161, 177–1786.CrossRefGoogle Scholar
  75. Smith, S.G., Lewis, M., Aschaffenburg, 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-lactalbumin at low resolution. Homology with lysozyme. Biochem. J. 242, 353–360.Google Scholar
  76. Stacey, A., Schnieke, A., Kerr, M., Scott, A., McKee, C., Cottingham, I., Binas, B., Wilde, C. and Colman, A. (1995). Lactation is disrupted by α-lactalbumin deficiency and can be restored by human α-lactalbumin gene replacement in mice. Proc. Natl. Acad. Sci. U.S.A. 92, 2835–2839.CrossRefGoogle Scholar
  77. Stinnakre, M.G., Vilotte, 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.CrossRefGoogle Scholar
  78. 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.CrossRefGoogle Scholar
  79. Svensson, M., Sabharwal, H., Hakansson, A., Mossberg, A.K., Lipniunas, P., Leffler, H., Svanborg, C. and Linse, S. (1999). Molecular characterization of α-lactalbumin folding variants that induce apoptosis in tumor cells. J. Biol. Chem. 274, 6388–6396.CrossRefGoogle Scholar
  80. Svensson, M., Hakansson, A., Mossberg, A.K., Linse, S. and Svanborg, C. (2000). Conversion of α-lactalbumin to a protein inducing apoptosis. Proc. Natl. Acad. Sci. U.S.A. 97, 4221–4226.CrossRefGoogle Scholar
  81. Svensson, M., Fast, J., Mossberg, A.K., Drunger, C., Gustafsson, L., Hallgren, O., Brooks, C.L., Berliner, L., Linse, S. and Svanborg, C. (2003). α-Lactalbumin unfolding is not sufficient to cause apoptosis, but is required for conversion to HAMLET (human α-lactalbumin made lethal to tumor cells). Protein Sci. 12, 2794–2804.CrossRefGoogle Scholar
  82. 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.Google Scholar
  83. Tolin, S., De Francheschi, G., Spolaore, B., Frare, E., Canton, M., Polverino de Laureto, P. and Fontana, A. (2010). The oleic acid complexes of proteolytic fragments of α-lactalbumin display apoptotic activity. FEBS J. 277, 163–173.CrossRefGoogle Scholar
  84. 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.Google Scholar
  85. Urashima, T., Saito, T., Nakamura, T. and Messer, M. (2002). Oligosaccharides of milk and colostrum in non-human mammals. Glycoconjugate J. 18, 357–371.CrossRefGoogle Scholar
  86. Urashima, T., Kobayashi, M., Asakuma, S., Uemura, Y., Arai, I., Fukuda, K., Saito, T., Mogoe, T., Ishikawa, H. and Fukui, Y. (2007). Chemical characterization of the oligosaccharides in Bryde’s whale (Balaenoptera edeni) and Sei whale (Balaenoptera borealis Lesson) milk. Comp. Biochem. Physiol. B, 146, 153–159.CrossRefGoogle Scholar
  87. Vilotte, J.L., Soulier, S., Mercier, J.-C., Gaye, P., Hue-Delahaie, D. and Furet, J.R. (1987). Complete nucleotide sequence of bovine α-lactalbumin gene: comparison with its rat counterpart. Biochimie, 69, 609–620.CrossRefGoogle Scholar
  88. Wheeler, M.B. (2003). Production of transgenic livestock: Promise fulfilled. J. Anim. Sci. 81, 32–37.Google Scholar
  89. Wilhelm, K., Darinskas, A., Noppe, W., Duchardt, E., Mok, K.H., Vukojević, V., Schleucher, J. and Morozova-Roche, L.A. (2009). Protein oligomerization induced by oleic acid at the solid–liquid interface—equine lysozyme cytotoxic complexes. FEBS J. 276, 3975–3989.CrossRefGoogle Scholar
  90. Zhang, K., Gao, R., Zhang, H., Cai, X., Shen, C., Wu, C., Zhao, S. and Yu, L. (2005). Molecular cloning and characterization of three novel lysozyme-like genes, predominantly expressed in the male reproductive system of humans, belonging to the c-type lysozyme/α-lactalbumin family. Biol. Reprod. 73, 1064–1071.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Department of Biomedical Science, Charles E. Schmidt College of MedicineFlorida Atlantic UniversityBoca RatonUSA

Personalised recommendations