Asynchronous Concurrent Secretion of Milk Proteins in the Tammar Wallaby (Macropus Eugenii)

  • Kevin R. Nicholas
  • Colin J. Wilde
  • Peter H. Bird
  • Kay A. K. Hendry
  • Karen Tregenza
  • Beverley Warner

Abstract

Lactation plays a central role in the reproductive cycle of all mammals. Eutherian species have evolved a lactational strategy that results in the birth of a relatively large young and whereas the milk provided to the young does not change significantly in composition, its synthesis and secretion is controlled by a complex interplay of endocrine, autocrine and paracrine influences (Topper and Freeman, 1980; Wilde and Peaker, 1990; Wilde et al., 1990; Streuli, 1993). In contrast to eutherian mammals, marsupials have adopted a reproductive strategy that includes a short gestation with the birth of an immature young. This is followed by extensive growth and physiological development of the dependent young during a comparatively long period of lactation (see Tyndale-Biscoe and Janssens, 1988). The need to provide the appropriate nutrition for this development requires that the lactating mother progressively alters the volume and composition of the milk made available to the sucking young (Green, 1984; Dove and Cork, 1989).

Keywords

Estrogen Lactate Cortisol Glucocorticoid Progesterone 

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References

  1. Addey, C.V.P., Peaker, M. and Wilde, C.J., 1991, Protein inhibitor which controls secretion of milk, U.K. Patent Application GB 2 238 052 A1.Google Scholar
  2. Addey, C.V.P., Peaker, M. and Wilde, C.J., 1992, Control of milk secretion, UK Patent Application GB 2 255 562 A1.Google Scholar
  3. Bird, P., Hendry, K.A.K., Shaw, D, Wilde, C. and Nicholas, K.R., 1994, Progressive changes in milk protein gene expression and prolactin binding during lactation in the tammar wallaby (Macropus eugenii). J. Mol. Endocrinol. 13:117.PubMedCrossRefGoogle Scholar
  4. Bird, P.H., Nicholas, K.R., Hendry, K.A.K. and Wilde, C.J., 1993, Asynchronous milk protein gene expression in lactating tammars, EAAP/ASAS Workshop on the Biology of Lactation in Farm Animals, Madrid, Elsevier Science Publishers, 35:189.Google Scholar
  5. Collet, C. and Joseph, R., 1993, A novel member of the lipocalin superfamily: tammar wallaby late lactation protein. Biochim. Biophys. Acta 1167:219.PubMedCrossRefGoogle Scholar
  6. Collet, C., Joseph, R. and, Nicholas, K.R., 1989, Molecular cloning and characterization of a novel marsupial milk protein gene. Biochem. Biophys. Res. Commun. 164:1380.PubMedCrossRefGoogle Scholar
  7. Collet, C., Joseph, R., and Nicholas, K.R., 1990, Cloning, cDNA analysis and prolactin-dependent expression of a marsupial ∝-lactalbumin. Rep. Fert. Dev. 2:693.CrossRefGoogle Scholar
  8. Collet, C., Joseph, R. and Nicholas, K.R., 1991, A marsupial ß-lactoglobulin gene: characterization and prolactin-dependent expression. J. Mol. Endocrinol. 6:9.PubMedCrossRefGoogle Scholar
  9. Collet, C., Joseph, R., and Nicholas, K.R., 1992, Molecular characterization and in vitro hormonal requirements for expression of two casein genes from a marsupial, J. Mol. Endocrinol. 8:1.CrossRefGoogle Scholar
  10. Dove, H. and Cork, S.J., 1989, Lactation in the tammar wallaby (Macropus eugenii). I. Milk consumption and the algebraic description of the lactation curve. J. Zool. London 219:385.CrossRefGoogle Scholar
  11. Findlay, L.,1982, The mammary glands of the tammar wallaby (Macropus eugenii) during pregnancy and lactation. J. Reprod. Fert. 65:59.CrossRefGoogle Scholar
  12. Findlay, L. and Renfree, M.B.,1984, Growth, development and secretion of the mammary gland of macropodid marsupials, in “Physiological Strategies in Lactation”, p. 403, Peaker, M., Vernon, R.G. and Knight, C.H., eds., Symposia of the Zoological Society of London, 51, Academic Press, London.Google Scholar
  13. Gaye, P., Hue-Delahaie, D., Mercier, J.C., Soulier, S., Vilotte, J.L., and Furet, J.P., 1986, Ovine ß- lactoglobulin messenger RNA: Nucleotide sequence and mRNA levels during functional differentiation of the mammary gland, Biochimie 68:1097.PubMedCrossRefGoogle Scholar
  14. Green, B., 1984, Composition of milk and energetics of growth in marsupials, in “Physiological Strategies in Lactation”, p. 369, Peaker, M., Vernon, R.G. and Knight, C.H., eds., Symposia of the Zoological Society of London, 51, Academic Press, London.Google Scholar
  15. Green, B. and Merchant, J., 1988, The composition of marsupial milk, in “The Developing Marsupial: Models for Biomedical Research,” p. 41, Tyndale-Biscoe, C.H. and Janssens, P.A., eds., Springer-Verlag, Heidelberg.CrossRefGoogle Scholar
  16. Harris, S., McClenaghan, M., Simons, J.P., Ali, S., and Clark, A.J., 1991, Developmental regulation of sheep ß-lactoglobulin gene in the mammary gland of transgenic mice, Devel. Gen. 12:299.CrossRefGoogle Scholar
  17. Hinds, L.A., 1988, Hormonal control of lactation, in “Physiological Strategies in Lactation”, p. 55, Peaker, M., Vernon, R.G. and Knight, C.H., eds., Symposia of the Zoological Society of London, 51, Academic Press, London.Google Scholar
  18. Hinds, L.A. and Tyndale-Biscoe, C.H., 1982a, Plasma progesterone levels in the pregnant and non-pregnant tammar, Macropus eugenii, J. Endocrinol. 93:99.PubMedCrossRefGoogle Scholar
  19. Hinds, L.A. and Tyndale-Biscoe, C.H., 1982b, Prolactin in the marsupial Macropus eugenii ,during the oestrus cycle, pregnancy and lactation, Biol. Reprod. 26:391.PubMedCrossRefGoogle Scholar
  20. Hobbs, A.A., Richards, D.A., Kessler, D.J., and Rosen, J.F., 1982, Complex hormonal regulation of rat casein gene expression, J. Biol. Chem. 257:3598.PubMedGoogle Scholar
  21. Joseph, R. and Collet, C., 1994, Double staining in situ study of mRNAs encoding milk proteins in the mammary gland of the tammar wallaby (Macropus eugenii). J. Reprod. Fert. 101:241.CrossRefGoogle Scholar
  22. Kuhn, N.J., 1977, Lactogenesis: the search for trigger mechanisms in different species, in “Comparative Aspects of Lactation”, p. 165, Peaker, M. ed., Academic Press, New York.Google Scholar
  23. Maher, F. and Nicholas, K.R., 1987, Pituitary-induced lactation in mammary gland explants from the pregnant tammar (Macropus eugenii): a negative role for cyclic AMP, Comp. Biochem. Physiol. 87A:1107.CrossRefGoogle Scholar
  24. Messer, M. and Elliott, C., 1987, Changes in ∝-lactalbumin, total lactose, UDP-galactose hydrolase and other factors in tammar wallaby (Macropus eugenii) milk during lactation, Aust. J. Biol. Sci. 40:37.Google Scholar
  25. Messer, M and Green, B, 1979, Milk carbohydrates of marsupials II. Quantitative and qualitative changes in milk carbohydrates during lactation in the tammar wallaby (Macropus eugenii), Aust. J. Biol. Sci. 32:519.PubMedGoogle Scholar
  26. Messer, M., Griffiths, M. and Green, B., 1984, Changes in milk carbohydrates and electrolytes during early lactation in the tammar wallaby, Macropus eugenii, Aust. J. Biol. Sci. 137:1.Google Scholar
  27. Messer, M. and Nicholas, K.R., 1991, Biosynthesis of marsupial milk oligosaccharides: characterization and developmental changes of two galactosyltransferases in lactating mammary glands of the tammar wallaby (Macropus eugenii), Biochim. Biophys. Acta 1077:79.PubMedCrossRefGoogle Scholar
  28. Nakhasi, H.L. and Qasba, P.K., 1979, Quantitation of milk proteins and their mRNAs in rat mammary gland at various stages of gestation and lactation, J. Biol. Chem. 254:6016.PubMedGoogle Scholar
  29. Nicholas, K.R., 1988a, Control of milk protein synthesis in the tammar wallaby: a model system to study prolactin-dependent development, in “The Developing Marsupial: Models for Biomedical Research”, p. 68, Tyndale-Biscoe, C.H. and Janssens, P.A., eds., Springer-Verlag, Heidelberg.CrossRefGoogle Scholar
  30. Nicholas, K.R., 1988b, Asynchronous dual lactation in a marsupial, the tammar wallaby (M. eugenii), Biochem. Biophys. Res. Comms. 154:529.CrossRefGoogle Scholar
  31. Nicholas, K.R., Collet, C., and Joseph, R., 1991, Hormone-responsive survival of mammary gland explants from the pregnant tammar (Macropus eugenii) in the absence of exogenous hormones and growth factors, Comp. Biochem. Physiol. 100A:163.CrossRefGoogle Scholar
  32. Nicholas, K.R., Messer, M., Elliott, C., Maher, F., and Shaw, D.C., 1987, A novel whey protein synthesized only in late lactation by the mammary gland from the tammar (Macropus eugenii), Biochem. J. 241:891.Google Scholar
  33. Nicholas, K. R. and Tyndale-Biscoe, C.H., 1985, Prolactin-dependent accumulation of ∝-lactalbumin in mammary gland explants from the pregnant tammar wallaby (Macropus eugenii), J. Endocrinol. 106:337.PubMedCrossRefGoogle Scholar
  34. Nicholas, K.R., Wilde, C.J., Bird, P.H., and Hendry, K.A.K., 1994, Asynchronous expression of milk protein genes during lactation in the tammar wallaby (Macropus eugenii), in “Comparative Biochemistry and Physiology. Research Trends”, Trivandrum, India.Google Scholar
  35. Oka, T., 1974, Spermidine in hormone-dependent differentiation of mammary gland in vitro, Science 184:78.PubMedCrossRefGoogle Scholar
  36. Rennison M.E., Kerr M., Addey C.V.P., Handel S.E., Turner M.D., Wilde C.J., and Burgoyne R.D., 1993, Inhibition of constitutive protein secretion from lactating mouse mammary epithelial cells by FIL (feedback inhibitor of lactation), a secreted milk protein, J. Cell Sci. 106:641.PubMedGoogle Scholar
  37. Stewart, F., 1984, Mammogenesis and changing prolactin receptor concentrations in the mammary glands of the tammar wallaby (Macropus eugenii), J. Reprod. Fert. 71:131.CrossRefGoogle Scholar
  38. Shamay, A., Pursei, V.G., Wall, R.J., and Hennighausen, L., 1992, Induction of lactogenesis in transgenic virgin pigs: evidence for gene and integration site-specific hormonal regulation, Mol. Endocrinol. 6:191.PubMedCrossRefGoogle Scholar
  39. Streuli, C. H., 1993, Extracellular matrix and gene expression in mammary epithelium, Sem. Cell Biol. 4:203.CrossRefGoogle Scholar
  40. Topper, Y.J. and Freeman, C.S., 1980, Multiple hormone interactions in the developmental biology of the mammary gland, Physiol. Rev. 60:1049.PubMedGoogle Scholar
  41. Tyndale-Biscoe, C.H. and Janssens, P.A., 1988, The Developing Marsupial: Models for Biomedical Research, Springer-Verlag, Heidelberg.CrossRefGoogle Scholar
  42. Vonderhaar, B.K., Bhattacharya, A., Alhadi, T., Liscia, D.S., Andrew, E.M., Young, J.K., Ginsburg, E., Bhattacharjee, M. and Horn, T.M., 1985, Isolation, characterization, and regulation of the prolactin receptor, J. Dairy Sci. 68:466.PubMedCrossRefGoogle Scholar
  43. Wilde, C.J., Addey, C.V.P., Boddy, L.M. and Peaker, M., 1995a, Autocrine inhibition of milk secretion by a protein in milk, Biochem. J., in press.Google Scholar
  44. Wilde, C.J., Calvert, D.T., Daly, A. and Peaker, M., 1987, The effects of goat milk fractions on synthesis of milk constituents by rabbit mammary explants and on milk yield in vivo: evidence for autocrine control of milk secretion, Biochem. J. 242:285.PubMedGoogle Scholar
  45. Wilde, C.J., Knight, C.H., Addey, C.V.P., Blatchford, D.R., Travers, M., Bennet, C.N. and Peaker, M., 1990a, Autocrine regulation of mammary cell differentiation, Protoplasma 159:112.CrossRefGoogle Scholar
  46. Wilde, C.J. and Peaker M., 1990b, Autocrine control in milk secretion. J. Agric. Sci. ,Cambridge 114:235.CrossRefGoogle Scholar
  47. Wilde, C.J., Prentice, A. and Peaker, M., 1995b, Breastfeeding: matching supply with demand in human lactation, Proc. Nutr. Soc., in press.Google Scholar

Copyright information

© Springer Science+Business Media New York 1995

Authors and Affiliations

  • Kevin R. Nicholas
    • 1
  • Colin J. Wilde
    • 2
  • Peter H. Bird
    • 1
    • 2
  • Kay A. K. Hendry
    • 2
  • Karen Tregenza
    • 1
    • 3
  • Beverley Warner
    • 1
    • 3
  1. 1.Division of Wildlife and EcologyCSIROLynehamAustralia
  2. 2.Hannah Research InstituteAyrUK
  3. 3.Division of Biochemistry and Molecular BiologyAustralian National UniversityCanberraAustralia

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