Abstract
Lactation is an important characteristic of mammalian reproduction sometimes referred to as the quintessence of mammals. Comparative genomics and transcriptomics experiments are allowing a more in-depth molecular analysis of the evolution of lactation throughout the mammalian kingdom and these recent results are reviewed here. Milk cell and mammary gland gene expression analysis with sequencing methodology have started to reveal conserved or specific milk protein and components of the lactation system of monotreme, marsupial and eutherian lineages. These experiments have confirmed the ancient origin of the complex lactation system and provided useful insight into the function of specific milk proteins in the control of the lactation programme or the role of milk in the regulation of growth and development of the young beyond simple nutritive aspects.
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Arnould JPY, Boyd IL (1995) Temporal patterns of milk production in Antarctic fur seals (Arctocephalus gazella). J Zool 237:1–12
Ballard FJ, Grbovac S, Nicholas KR, Owens PC, Read LC (1995) Differential changes in the milk concentrations of epidermal growth factor and insulin-like growth factor-I during lactation in the tammar wallaby, Macropus eugenii. Gen Comp Endocrinol 98:262–268
Bininda-Emonds OR, Cardillo M, Jones KE, MacPhee RD, Beck RM et al (2007) The delayed rise of present-day mammals. Nature 446:507–512
Bird PH, Hendry KA, Shaw DC, Wilde CJ, Nicholas KR (1994) Progressive changes in milk protein gene expression and prolactin binding during lactation in the tammar wallaby (Macropus eugenii). J Mol Endocrinol 13:117–125
Bonner WN (1984) Lactation strategies in pinnipeds: problems for a marine mammalian group. Symp Zool Soc Lond 51:253–272
Brennan AJ, Sharp JA, Digby MR, Nicholas KR (2007) The tammar wallaby: a model to examine endocrine and local control of lactation. IUBMB Life 59:146–150
Brennan AJ, Sharp JA, Lefevre CM, Nicholas KR (2008) Uncoupling the mechanisms that facilitate cell survival in hormone-deprived bovine mammary explants. J Mol Endocrinol 41:103–116
Demmer J, Stasiuk SJ, Grigor MR, Simpson KJ, Nicholas KR (2001) Differential expression of the whey acidic protein gene during lactation in the brushtail possum (Trichosurus vulpecula). Biochim Biophys Acta 1522:187–194
Elsik CG, Tellam RL, Worley KC, Gibbs RA, Muzny DM et al (2009) The genome sequence of taurine cattle: a window to ruminant biology and evolution. Science 324:522–528
Findlay L (1982) The mammary glands of the tammar wallaby (Macropus eugenii) during pregnancy and lactation. J Reprod Fertil 65:59–66
Fordyce RE (ed) (2002) Fossil record. Academic Press, San Diego, California, USA, pp 453–471
Green B, Newgrain K, Merchant J (1980) Changes in milk composition during lactation in the tammar wallaby (Macropus eugenii). Aust J Biol Sci 33:35–42
Green B, Griffiths M, Leckie RM (1983) Qualitative and quantitative changes in milk fat during lactation in the tammar wallaby (Macropus eugenii). Aust J Biol Sci 36:455–461
Green B, VandeBerg JL, Newgrain K (1991) Milk composition in an American marsupial (Monodelphis domestica). Comp Biochem Physiol B 99:663–665
Griffiths M (1978) The biology of monotremes. Academic Press, New York, NY
Guss JM, Messer M, Costello M, Hardy K, Kumar V (1997) Structure of the calcium-binding echidna milk lysozyme at 1.9 A resolution. Acta Crystallogr D Biol Crystallogr 53:355–363
Hajjoubi S, Rival-Gervier S, Hayes H, Floriot S, Eggen A et al (2006) Ruminants genome no longer contains whey acidic protein gene but only a pseudogene. Gene 370:104–112
Hendry KA, Simpson KJ, Nicholas KR, Wilde CJ (1998) Autocrine inhibition of milk secretion in the lactating tammar wallaby (Macropus eugenii). J Mol Endocrinol 21:169–177
Hennighausen LG, Sippel AE (1982) Characterization and cloning of the mRNAs specific for the lactating mouse mammary gland. Eur J Biochem 125:131–141
Hopper KE, McKenzie HA (1974) Comparative studies of alpha-lactalbumin and lysozyme: echidna lysozyme. Mol Cell Biochem 3:93–108
Jenness R (1986) Lactational performance of various mammalian species. J Dairy Sci 69:869–885
Jones WK, Yu-Lee LY, Clift SM, Brown TL, Rosen JM (1985) The rat casein multigene family. Fine structure and evolution of the beta-casein gene. J Biol Chem 260:7042–7050
Joseph M, Griffiths M (1992) Whey proteins in milks of monotremes and wallabies. Australian Mammology 14:125–127
Kawasaki K, Weiss KM (2003) Mineralized tissue and vertebrate evolution: the secretory calcium-binding phosphoprotein gene cluster. Proc Natl Acad Sci USA 100:4060–4065
Lefevre CM, Digby MR, Whitley JC, Strahm Y, Nicholas KR (2007) Lactation transcriptomics in the australian marsupial, Macropus eugenii: transcript sequencing and quantification. BMC Genomics 8:417
Lefevre CM, Sharp JA, Nicholas KR (2009) Characterisation of monotreme caseins reveals lineage-specific expansion of an ancestral casein locus in mammals. Reprod Fertil Dev 21:1015–1027
Lemay DG, Neville MC, Rudolph MC, Pollard KS, German JB (2007) Gene regulatory networks in lactation: identification of global principles using bioinformatics. BMC Syst Biol 1:56
Lemay DG, Lynn DJ, Martin WF, Neville MC, Casey TM et al (2009) The bovine lactation genome: insights into the evolution of mammalian milk. Genome Biol 10:R43
Lemon M, Bailey LF (1966) A specific protein difference in the milk from two mammary glands of a red kangaroo. Aust J Exp Biol Med Sci 44:705–707
Li M, Liu X, Robinson G, Bar-Peled U, Wagner KU et al (1997) Mammary-derived signals activate programmed cell death during the first stage of mammary gland involution. Proc Natl Acad Sci USA 94:3425–3430
Madsen O (2009) Mammals (mammalia). In: Hedges SB, Kumar SB (eds) The timetree of life. Oxford Univeristy Press, Oxford, pp 459–461
Maningat PD, Sen P, Sunehag AL, Hadsell DL, Haymond MW (2007) Regulation of gene expression in human mammary epithelium: effect of breast pumping. J Endocrinol 195:503–511
Menzies KK, Lee HJ, Lefevre C, Ormandy CJ, Macmillan KL, Nicholas KR (2009a) Insulin, a key regulator of hormone responsive milk protein synthesis during lactogenesis in murine mammary explants. Funct Integr Genomics 10(1):87–95
Menzies KK, Lefevre C, Macmillan KL, Nicholas KR (2009b) Insulin regulates milk protein synthesis at multiple levels in the bovine mammary gland. Funct Integr Genomics 9:197–217
Menzies KK, Lefevre C, Sharp JA, Macmillan KL, Sheehy PA, Nicholas KR (2009c) A novel approach identified the FOLR1 gene, a putative regulator of milk protein synthesis. Mamm Genome 20:498–503
Mercier JC, Chobert JM, Addeo F (1976) Comparative study of the amino acid sequences of the caseinomacropeptides from seven species. FEBS Lett 72:208–214
Messer M, Elliott C (1987) Changes in alpha-lactalbumin, total lactose, UDP-galactose hydrolase and other factors in tammar wallaby (Macropus eugenii) milk during lactation. Aust J Biol Sci 40:37–46
Messer M, Griffiths M, Rismiller PD, Shaw DC (1997) Lactose synthesis in a monotreme, the echidna (Tachyglossus aculeatus): isolation and amino acid sequence of echidna alpha-lactalbumin. Comp Biochem Physiol B Biochem Mol Biol 118:403–410
Mori Y, Hiraki Y, Shukunami C, Kakudo S, Shiokawa M et al (1997) Stimulation of osteoblast proliferation by the cartilage-derived growth promoting factors chondromodulin-I and -II. FEBS Lett 406:310–314
Murphy LC, Tsuyuki D, Myal Y, Shiu RP (1987) Isolation and sequencing of a cDNA clone for a prolactin-inducible protein (PIP). Regulation of PIP gene expression in the human breast cancer cell line, T-47D. J Biol Chem 262:15236–15241
Nicholas KR (1988) Asynchronous dual lactation in a marsupial, the tammar wallaby (Macropus eugenii). Biochem Biophys Res Commun 154:529–536
Nicholas KR, Messer M, Elliott C, Maher F, Shaw DC (1987) A novel whey protein synthesized only in late lactation by the mammary gland from the tammar (Macropus eugenii). Biochem J 241:899–904
Nicholas K, Simpson K, Wilson M, Trott J, Shaw D (1997) The tammar wallaby: a model to study putative autocrine-induced changes in milk composition. J Mammary Gland Biol Neoplasia 2:299–310
Nicholas KR, Fisher JA, Muths E, Trott J, Janssens PA et al (2001) Secretion of whey acidic protein and cystatin is down regulated at mid-lactation in the red kangaroo (Macropus rufus). Comp Biochem Physiol A Mol Integr Physiol 129:851–858
Oftedal OT, Boness DJ, Tedmam RA (1987) The behaviour, physiology, and anatomy of lactation in the Pinnipedia. Curr Mammal 1:175–245
Peaker M (2002) The mammary gland in mammalian evolution: a brief commentary on some of the concepts. J Mammary Gland Biol Neoplasia 7:347–353
Piotte CP, Hunter AK, Marshall CJ, Grigor MR (1998) Phylogenetic analysis of three lipocalin-like proteins present in the milk of Trichosurus vulpecula (Phalangeridae, Marsupialia). J Mol Evol 46:361–369
Rijnkels M (2002) Multispecies comparison of the casein gene loci and evolution of casein gene family. J Mammary Gland Biol Neoplasia 7:327–345
Rudolph MC, McManaman JL, Hunter L, Phang T, Neville MC (2003) Functional development of the mammary gland: use of expression profiling and trajectory clustering to reveal changes in gene expression during pregnancy, lactation, and involution. J Mammary Gland Biol Neoplasia 8:287–307
Sharp JA, Cane KN, Lefevre C, Arnould JP, Nicholas KR (2006) Fur seal adaptations to lactation: insights into mammary gland function. Curr Top Dev Biol 72:275–308
Sharp JA, Lefevre C, Nicholas KR (2007) Molecular evolution of monotreme and marsupial whey acidic protein genes. Evol Dev 9:378–392
Sharp JA, Lefevre C, Nicholas KR (2008) Lack of functional alpha-lactalbumin prevents involution in cape fur seals and identifies the protein as an apoptotic milk factor in mammary gland involution. BMC Biol 6:48
Shaw DC, Messer M, Scrivener AM, Nicholas KR, Griffiths M (1993) Isolation, partial characterisation, and amino acid sequence of alpha-lactalbumin from platypus (Ornithorhynchus anatinus) milk. Biochim Biophys Acta 1161:177–186
Simpson K, Shaw D, Nicholas K (1998) Developmentally-regulated expression of a putative protease inhibitor gene in the lactating mammary gland of the tammar wallaby, Macropus eugenii. Comp Biochem Physiol B Biochem Mol Biol 120:535–541
Tolin S, De Franceschi G, Spolaore B, Frare E, Canton M et al (2009) The oleic acid complexes of proteolytic fragments of alpha-lactalbumin display apoptotic activity. FEBS J 277(1):163–173
Topcic D, Auguste A, De Leo AA, Lefevre C, Digby MR, Nicholas KR (2009) Characterization of the tammar wallaby (Macropus eugenii) whey acidic protein gene: new insights into the function of the protein. Evol Dev 11:363–375
Trott JF, Wilson MJ, Hovey RC, Shaw DC, Nicholas KR (2002) Expression of novel lipocalin-like milk protein gene is developmentally-regulated during lactation in the tammar wallaby, Macropus eugenii. Gene 283:287–297
Trott JF, Simpson KJ, Moyle RL, Hearn CM, Shaw G et al (2003) Maternal regulation of milk composition, milk production, and pouch young development during lactation in the tammar wallaby (Macropus eugenii). Biol Reprod 68:929–936
Tyndale-Biscoe H, Janssens PA, Australian Academy of Science, Australian Society for Reproductive Biology, Australian Mammal Society (1988) The developing marsupial: models for biomedical research, vol viii. Springer-Verlag, Berlin, p 245
Waite R, Giraud A, Old J, Howlett M, Shaw G et al (2005) Cross-fostering in Macropus eugenii leads to increased weight but not accelerated gastrointestinal maturation. J Exp Zool 303:331–344
Warren WC, Hillier LW, Marshall Graves JA, Birney E, Ponting CP et al (2008) Genome analysis of the platypus reveals unique signatures of evolution. Nature 453:175–183
Yamagoe S, Mizuno S, Suzuki K (1998) Molecular cloning of human and bovine LECT2 having a neutrophil chemotactic activity and its specific expression in the liver. Biochim Biophys Acta 1396:105–113
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Lefèvre, C.M., Menzies, K., Sharp, J.A., Nicholas, K.R. (2010). Comparative Genomics and Transcriptomics of Lactation. In: Pontarotti, P. (eds) Evolutionary Biology – Concepts, Molecular and Morphological Evolution. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-12340-5_7
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DOI: https://doi.org/10.1007/978-3-642-12340-5_7
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