The evolution of genomic imprinting: Epigenetic control of mammary gland development and postnatal resource control

Focus Article

Anne C. Ferguson‐Smith, Geula Hanin

Published Online: Dec 26 2019

DOI: 10.1002/wsbm.1476

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Abstract Genomic imprinting is an epigenetically regulated process leading to gene expression according to its parental origin. Imprinting is essential for prenatal growth and development, regulating nutritional resources to offspring, and contributing to a favored theory about the evolution of imprinting being due to a conflict between maternal and paternal genomes for the control of prenatal resources—the so‐called kinship hypothesis. Genomic imprinting has been mainly studied during embryonic and placental development; however, maternal nutrient provisioning is not restricted to the prenatal period. In this context, the mammary gland acts at the maternal‐offspring interface providing milk to the newborn. Maternal care including lactation supports the offspring, delivering nutrients and bioactive molecules protecting against infections and contributing to healthy organ development and immune maturation. The normal developmental cycle of the mammary gland—pregnancy, lactation, involution—is vital for this process, raising the question of whether genomic imprinting might also play a role in postnatal nutrient transfer by controlling mammary gland development. Characterizing the function and epigenetic regulation of imprinted genes in the mammary gland cycle may therefore provide novel insights into the evolution of imprinting since the offspring's paternal genome is absent from the mammary gland, in addition to increasing our knowledge of postnatal nutrition and its relation to life‐long health. This article is categorized under: Developmental Biology > Developmental Processes in Health and Disease

Illustration of the developmental cycle of the adult mammary gland, initiated from the adult virgin state (top), where tertiary structures of mammary ducts populate the mammary fat pad, represented as a gray circle. During pregnancy, upon the exposure to circulating hormones like Progesterone and Prolactin, the mammary gland differentiates to form milk‐producing alveoli (right) which will become functional after parturition. During lactation, the mammary gland becomes fully populated by alveoli to produce milk, this is mostly regulated by prolactin (bottom). Upon cessation of lactation, Involution begins (left) and a two‐stage process is initiated, removing milk‐producing alveoli and remodeling of the tissue back to a simple ductal architecture

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Diagram illustrating the common features of the placenta and mammary gland. These organs function pre‐ and postnatally respectively to provide the ultimate support to the offspring

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Schematic representation of genomic imprinting. Paternal chromosome is blue, maternal is pink. The unmethylated regulatory regions are represented as white circles, and methylation as dark gray circles. The Dlk1‐Dio3 imprinted domain is shown as an example, it is comprised of Meg3 and multiple small‐noncoding RNA that are expressed from the maternally inherited chromosome, and three protein‐coding genes, Dlk1, Rtl1, and Dio3 that are expressed from the paternal chromosome. Arrows indicate the direction of transcription

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(a) A schematic representation of the various cell types comprising the adult mammary gland. (b) Table showing the currently available data on imprinted gene expression in mammary gland cells, allelic expression in the mammary gland if available and the relevant reference. Background color represents the corresponding cell type in (a). White background represents information which does not refer to a single cell type

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References

Abu‐Amero,, S., Monk,, D., Frost,, J., Preece,, M., Stanier,, P., & Moore,, G. E. (2008). The genetic aetiology of Silver‐Russell syndrome. Journal of Medical Genetics, 45(4), 193–199. https://doi.org/10.1136/jmg.2007.053017
Andergassen,, D., Dotter,, C. P., Wenzel,, D., Sigl,, V., Bammer,, P. C., Muckenhuber,, M., … Hudson,, Q. J. (2017). Mapping the mouse allelome reveals tissue‐specific regulation of allelic expression. eLife, 6(Xci), 1–29. https://doi.org/10.7554/eLife.25125
Aydin,, S., Kuloglu,, T., & Aydin,, S. (2013). Copeptin, adropin and irisin concentrations in breast milk and plasma of healthy women and those with gestational diabetes mellitus. Peptides, 47, 66–70. https://doi.org/10.1016/j.peptides.2013.07.001
Bach,, K., Pensa,, S., Grzelak,, M., Hadfield,, J., Adams,, D. J., Marioni,, J. C., & Khaled,, W. T. (2017). Differentiation dynamics of mammary epithelial cells revealed by single‐cell RNA sequencing. Nature Communications, 8(1), 2128. https://doi.org/10.1038/s41467-017-02001-5
Ballard,, O., & Morrow,, A. L. (2013). Human milk composition. Nutrients and bioactive factors. Pediatric Clinics of North America, 60(1), 49–74. https://doi.org/10.1016/j.pcl.2012.10.002
Barlow,, D. P. (2011). Genomic imprinting: a mammalian epigenetic discovery model. Annual Review of Genetics, 45(1), 379–403. https://doi.org/10.1146/annurev-genet-110410-132459
Bartolomei,, M. S., & Ferguson‐Smith,, A. C. (2011). Mammalian genomic imprinting. Cold Spring Harbor Perspectives in Biology, 3(7), 1–17. https://doi.org/10.1101/cshperspect.a002592
Bogutz,, A. B., Oh‐McGinnis,, R., Jacob,, K. J., Ho‐Lau,, R., Gu,, T., Gertsenstein,, M., … Lefebvre,, L. (2018). Transcription factor ASCL2 is required for development of the glycogen trophoblast cell lineage. PLoS Genetics, 14(8), 1–26. https://doi.org/10.1371/journal.pgen.1007587
Boström,, P., Wu,, J., Jedrychowski,, M. P., Korde,, A., Ye,, L., Lo,, J. C., … Spiegelman,, B. M. (2012). A PGC1‐α‐dependent myokine that drives brown‐fat‐like development of white fat and thermogenesis. Nature, 481(7382), 463–468. https://doi.org/10.1038/nature10777
Brisken,, C., Ayyannan,, A., Nguyen,, C., Heineman,, A., Reinhardt,, F., Jan,, T., … Weinberg,, R. A. (2002). IGF‐2 is a mediator of prolactin‐induced morphogenesis in the breast. Developmental Cell, 3(6), 877–887. https://doi.org/10.1016/S1534-5807(02)00365-9
Brisken,, C., & O`Malley,, B. (2010). Hormone action in the mammary gland. Cold Spring Harbor Perspectives in Biology, 2(12), 1–15. https://doi.org/10.1101/cshperspect.a003178
Champagne,, F. A., Curley,, J. P., Swaney,, W. T., Hasen,, N. S., & Keverne,, E. B. (2009). Paternal influence on female behavior: The role of Peg3 in exploration, olfaction, and neuroendocrine regulation of maternal behavior of female mice. Behavioral Neuroscience, 123(3), 469–480. https://doi.org/10.1037/a0015060
Chen,, M., Berger,, A., Kablan,, A., Zhang,, J., Gavrilova,, O., & Weinstein,, L. S. (2012). G s α deficiency in the paraventricular nucleus of the hypothalamus partially contributes to obesity associated with G s α mutations. Endocrinology, 153(9), 4256–4265. https://doi.org/10.1210/en.2012-1113
Chen,, M., Gavrilova,, O., Liu,, J., Xie,, T., Deng,, C., Nguyen,, A. T., … Weinstein,, L. S. (2005). Alternative Gnas gene products have opposite effects on glucose and lipid metabolism. Proceedings of the National Academy of Sciences of the United States of America, 102(20), 7386–7391. https://doi.org/10.1073/pnas.0408268102
Cleaton,, M. A. M., Dent,, C. L., Howard,, M., Corish,, J. A., Gutteridge,, I., Sovio,, U., … Charalambous,, M. (2016). Fetus‐derived DLK1 is required for maternal metabolic adaptations to pregnancy and is associated with fetal growth restriction. Nature Genetics, 48(12), 1473–1480. https://doi.org/10.1038/ng.3699
Cleaton,, M. A. M., Edwards,, C. A., & Ferguson‐Smith,, A. C. (2014). Phenotypic outcomes of imprinted gene models in mice: Elucidation of pre‐ and postnatal functions of imprinted genes. Annual Review of Genomics and Human Genetics, 15(1), 93–126. https://doi.org/10.1146/annurev-genom-091212-153441
Coan,, P. M., Burton,, G. J., & Ferguson‐Smith,, A. C. (2005). Imprinted genes in the placenta—a review. Placenta, 26(Suppl.), 10–20. https://doi.org/10.1016/j.placenta.2004.12.009
Constância,, M., Hemberger,, M., Hughes,, J., Dean,, W., Ferguson‐Smith,, A., Fundele,, R., … Reik,, W. (2002). Placental‐specific IGF‐II is a major modulator of placental and fetal growth. Nature, 417(6892), 945–948. https://doi.org/10.1038/nature00819
Cowley,, M., Garfield,, A. S., Madon‐Simon,, M., Charalambous,, M., Clarkson,, R. W., Smalley,, M. J., … Ward,, A. (2014). Developmental programming mediated by complementary roles of imprinted Grb10 in mother and pup. PLoS Biology, 12(2), e1001799. https://doi.org/10.1371/journal.pbio.1001799
Cubero,, J., Valero,, V., Sánchez,, J., Rivero,, M., Parvez,, H., Rodríquez,, A. B., & Barriga Ibars,, C. (2005). The circadian rhythm of tryptophan in breast milk affects the rhythms of 6‐sulfatoxymelatonin and sleep in newborn. Neuroendocrinology Letters, 26(6), 657–661.
Curley,, J. P., Barton,, S., Surani,, A., & Keverne,, E. B. (2004). Coadaptation in mother and infant regulated by a paternally expressed imprinted gene. Proceedings of the Royal Society B: Biological Sciences, 271(1545), 1303–1309. https://doi.org/10.1098/rspb.2004.2725
De Silva,, D., Kunasegaran,, K., Ghosh,, S., & Pietersen,, A. M. (2015). Transcriptome analysis of the hormone‐sensing cells in mammary epithelial reveals dynamic changes in early pregnancy. BMC Developmental Biology, 15(1), 1–14. https://doi.org/10.1186/s12861-015-0058-9
Denizot,, A. L., Besson,, V., Correra,, R. M., Mazzola,, A., Lopes,, I., Courbard,, J. R., … Sassoon,, D. A. (2016). A novel mutant allele of Pw1/Peg3 does not affect maternal behavior or nursing behavior. PLoS Genetics, 12(5), 1–20. https://doi.org/10.1371/journal.pgen.1006053
Dravis,, C., Chung,, C. Y., Lytle,, N. K., Herrera‐Valdez,, J., Luna,, G., Trejo,, C. L., … Wahl,, G. M. (2018). Epigenetic and transcriptomic profiling of mammary gland development and tumor models disclose regulators of cell state plasticity. Cancer Cell, 34(3), 466–482.e6. https://doi.org/10.1016/j.ccell.2018.08.001
Ferguson‐Smith,, A. C. (2011). Genomic imprinting: The emergence of an epigenetic paradigm. Nature Reviews Genetics, 12(8), 565–575. https://doi.org/10.1038/nrg3032
Fernández‐Rebollo,, E., Maeda,, A., Reyes,, M., Turan,, S., Fröhlich,, L. F., Plagge,, A., … Bastepe,, M. (2012). Loss of XLαs (extra‐large αs) imprinting results in early postnatal hypoglycemia and lethality in a mouse model of pseudohypoparathyroidism Ib. Proceedings of the National Academy of Sciences, 109(17), 6638–6643. https://doi.org/10.1073/pnas.1117608109
Frey,, W. D., & Kim,, J. (2015). Tissue‐specific contributions of paternally expressed gene 3 in lactation and maternal care of Mus musculus. PLoS One, 10(12), 1–16. https://doi.org/10.1371/journal.pone.0144459
Frey,, W. D., Sharma,, K., Cain,, T. L., Nishimori,, K., Teruyama,, R., & Kim,, J. (2018). Oxytocin receptor is regulated by Peg3. PLoS One, 13(8), 1–12 https://doi.org/10.1371/journal.pone.0202476
Fu,, N. Y., Rios,, A. C., Pal,, B., Soetanto,, R., Lun,, A. T. L., Liu,, K., … Visvader,, J. E. (2015). EGF‐mediated induction of Mcl‐1 at the switch to lactation is essential for alveolar cell survival. Nature Cell Biology, 17(4), 365–375. https://doi.org/10.1038/ncb3117
Gavaldà‐Navarro,, A., Hondares,, E., Giralt,, M., Mampel,, T., Iglesias,, R., & Villarroya,, F. (2015). Fibroblast growth factor 21 in breast milk controls neonatal intestine function. Scientific Reports, 5, 1–13. https://doi.org/10.1038/srep13717
Gersting,, J. A., Kotto‐Kome,, C. A., Du,, Y., Christensen,, R. D., & Calhoun,, D. A. (2003). Bioavailability of granulocyte colony‐stimulating factor administered enterally to suckling mice. Pharmacological Research, 48(6), 643–647. https://doi.org/10.1016/S1043-6618(03)00249-4
Gjorevski,, N., & Nelson,, C. M. (2011). Integrated morphodynamic signalling of the mammary gland. Nature Reviews. Molecular Cell Biology, 12(9), 581–593. https://doi.org/10.1038/nrm3168
Goovaerts,, T., Steyaert,, S., Vandenbussche,, C. A., Galle,, J., Thas,, O., Van Criekinge,, W., & De Meyer,, T. (2018). A comprehensive overview of genomic imprinting in breast and its deregulation in cancer. Nature Communications, 9, 4120. https://doi.org/10.1038/s41467-018-06566-7
Gude,, N. M., Roberts,, C. T., Kalionis,, B., & King,, R. G. (2004). Growth and function of the normal human placenta. Thrombosis Research, 114(5–6 Special Issue), 397–407. https://doi.org/10.1016/j.thromres.2004.06.038
Gura,, T. (2014). Nature`s first functional food. Science, 345(6198), 747–749. https://doi.org/10.1126/science.345.6198.747
Hager,, R., & Johnstone,, R. A. (2003). The genetic basis of family conflict resolution in mice. Nature, 421(6922), 533–535. https://doi.org/10.1038/nature01239
Haig,, D. (2000). The kinship theory of genomic imprinting. Annual Review of Ecology and Systematics, 34, 9–32.
Haig,, D., & Westoby,, M. (1991). Genomic imprinting in endosperm: Its effect on seed development in crosses between species, and between different ploidies of the same species, and its implications for the evolution of apomixis. Philosophical Transactions of the Royal Society B: Biological Sciences, 333. http://doi.org/10.1098/rstb.1991.0057
Hassiotou,, F., Beltran,, A., Chetwynd,, E., Stuebe,, A. M., Twigger,, A. J., Metzger,, P., … Hartmann,, P. E. (2012). Breastmilk is a novel source of stem cells with multilineage differentiation potential. Stem Cells, 30(10), 2164–2174. https://doi.org/10.1002/stem.1188
Hassiotou,, F., Hepworth,, A. R., Metzger,, P., Lai,, C. T., Trengove,, N., Hartmann,, P. E., & Filgueira,, L. (2013). Maternal and infant infections stimulate a rapid leukocyte response in breastmilk. Clinical %26 Translational Immunology, 2(4), e3. https://doi.org/10.1038/cti.2013.1
Hennet,, T., & Borsig,, L. (2016). Breastfed at Tiffany`s. Trends in Biochemical Sciences, 41(6), 508–518. https://doi.org/10.1016/j.tibs.2016.02.008
Hernandez,, A., Garcia,, B., & Obregon,, M. J. (2007). Gene expression from the imprinted Dio3 locus is associated with cell proliferation of cultured brown adipocytes. Endocrinology, 148(8), 3968–3976. https://doi.org/10.1210/en.2007-0029
Horsthemke,, B., & Buiting,, K. (2006). Imprinting defects on human chromosome 15. Cytogenetic and Genome Research, 113(1–4), 292–299. https://doi.org/10.1159/000090844
Huh,, S. J., Clement,, K., Jee,, D., Merlini,, A., Choudhury,, S., Maruyama,, R., … Polyak,, K. (2015). Age‐ and pregnancy‐associated dna methylation changes in mammary epithelial cells. Stem Cell Reports, 4(2), 297–311. https://doi.org/10.1016/j.stemcr.2014.12.009
Hurtado,, C. W., Golden‐Mason,, L., Brocato,, M., Krull,, M., Narkewicz,, M. R., & Rosen,, H. R. (2010). Innate immune function in placenta and cord blood of hepatitis C—seropositive mother–infant dyads. PLoS One, 5(8), 1–8. https://doi.org/10.1371/journal.pone.0012232
Illnerová,, H., Buresová,, M., & Presl,, J. (1993). Melatonin rhythm in human milk. The Journal of Clinical Endocrinology %26 Metabolism, 77(3), 838–841.
Ishida,, M., & Moore,, G. E. (2013). The role of imprinted genes in humans. Molecular Aspects of Medicine, 34(4), 826–840. https://doi.org/10.1016/j.mam.2012.06.009
Ito,, M., Sferruzzi‐Perri,, A. N., Edwards,, C. A., Adalsteinsson,, B. T., Allen,, S. E., Loo,, T.‐H., … Ferguson‐Smith,, A. C. (2015). A trans‐homologue interaction between reciprocally imprinted miR‐127 and Rtl1 regulates placenta development. Development (Cambridge), 142(14), 2425–2430. https://doi.org/10.1242/dev.121996
Jonker,, J. W., Wagenaar,, E., van Eijl,, S., & Schinkel,, A. H. (2003). Deficiency in the organic cation transporters 1 and 2 (Oct1/Oct2 [Slc22a1/Slc22a2]) in mice abolishes renal secretion of organic cations. Molecular and Cellular Biology, 23(21), 7902–7908. https://doi.org/10.1128/mcb.23.21.7902-7908.2003
Klenke,, S., Siffert,, W., & Frey,, U. H. (2011). A novel aspect of GNAS imprinting: Higher maternal expression of Gαs in human lymphoblasts, peripheral blood mononuclear cells, mammary adipose tissue, and heart. Molecular and Cellular Endocrinology, 341(1–2), 63–70. https://doi.org/10.1016/j.mce.2011.05.032
Koldovsky,, O. (1994). Hormonally active peptides in human milk. Acta Paediatrica, 83(402), 89–93.
Kosaka,, N., Izumi,, H., Sekine,, K., & Ochiya,, T. (2010). microRNA as a new immune‐regulatory agent in breast milk extraction of RNAs and expression analysis existence of microvesicles. Silence, 1(7), 8. https://doi.org/10.1186/1758-907X-1-7
Lefebvre,, L., Viville,, S., Barton,, S. C., Ishino,, F., Keverne,, E. B., & Surani,, M. a. (1998). Abnormal maternal behaviour and growth retardation associated with loss of the imprinted gene Mest. Nature Genetics, 20(2), 163–169. https://doi.org/10.1038/2464
Lim,, E., Wu,, D., Pal,, B., Bouras,, T., Asselin‐Labat,, M. L., Vaillant,, F., … Visvader,, J. E. (2010). Transcriptome analyses of mouse and human mammary cell subpopulations reveal multiple conserved genes and pathways. Breast Cancer Research, 12, R21. https://doi.org/10.1186/bcr2560
Liu,, J., Litman,, D., Rosenberg,, M. J., Yu,, S., Biesecker,, L. G., & Weinstein,, L. S. (2000). A GNAS1 imprinting defect in pseudohypoparathyroidism type IB. Journal of Clinical Investigation, 106(9), 1167–1174. https://doi.org/10.1172/JCI10431
Macias,, H., & Hinck,, L. (2012). Mammary gland development. Wiley Interdisciplinary Reviews: Developmental Biology, 1(4), 533–557. https://doi.org/10.1002/wdev.35
Mackay,, D. J. G., Callaway,, J. L. A., Marks,, S. M., White,, H. E., Acerini,, C. L., Boonen,, S. E., … Temple,, I. K. (2008). Hypomethylation of multiple imprinted loci in individuals with transient neonatal diabetes is associated with mutations in ZFP57. Nature Genetics, 40(8), 949–951. https://doi.org/10.1038/ng.187
Manca,, S., Upadhyaya,, B., Mutai,, E., Desaulniers,, A. T., Cederberg,, R. A., White,, B. R., & Zempleni,, J. (2018). Milk exosomes are bioavailable and distinct microRNA cargos have unique tissue distribution patterns. Scientific Reports, 8(1), 1–11. https://doi.org/10.1038/s41598-018-29780-1
Martin‐Gronert,, M. S., & Ozanne,, S. E. (2012). Mechanisms underlying the developmental origins of disease. Reviews in Endocrine and Metabolic Disorders, 13(2), 85–92. https://doi.org/10.1007/s11154-012-9210-z
Melnik,, B. C., John,, S. M., & Schmitz,, G. (2013). Milk is not just food but most likely a genetic transfection system activating mTORC1 signaling for postnatal growth. Nutrition Journal, 12(1), 1–10. https://doi.org/10.1186/1475-2891-12-103
Michalak,, E. M., Milevskiy,, M. J. G., Joyce,, R. M., Dekkers,, J. F., Jamieson,, P. R., Pal,, B., … Visvader,, J. E. (2018). Canonical PRC2 function is essential for mammary gland development and affects chromatin compaction in mammary organoids. PLoS Biology, 16(8), 1–21. https://doi.org/10.1371/journal.pbio.2004986
Moore,, T., & Haig,, D. (1991). Genomic imprinting in mammalian development: A parental tug‐of‐war. Trends in Genetics, 7(2), 45–49. https://doi.org/10.1016/0168-9525(91)90230-N
Mor,, G., & Cardenas,, I. (2011). The immune system in pregnancy. American Journal of Reproductive Immunology, 63(6), 425–433. https://doi.org/10.1111/j.1600-0897.2010.00836.x.The
Moran‐Lev,, H., Mimouni,, F. B., Ovental,, A., Mangel,, L., Mandel,, D., & Lubetzky,, R. (2015). Circadian macronutrients variations over the first 7 weeks of human milk feeding of preterm infants. Breastfeeding Medicine, 10(7), 366–370. https://doi.org/10.1089/bfm.2015.0053
Munch,, E. M., Harris,, R. A., Mohammad,, M., Benham,, A. L., Pejerrey,, S. M., Showalter,, L., … Aagaard,, K. (2013). Transcriptome profiling of microRNA by next‐gen deep sequencing reveals known and novel miRNA species in the lipid fraction of human breast Milk. PLoS One, 8(2), e50564. https://doi.org/10.1371/journal.pone.0050564
Murphy,, V. E., Smith,, R., Giles,, W. B., & Clifton,, V. L. (2006). Endocrine regulation of human fetal growth: The role of the mother, placenta, and fetus. Endocrine Reviews, 27(2), 141–169. https://doi.org/10.1210/er.2005-0011
Pal,, B., Bouras,, T., Shi,, W., Vaillant,, F., Sheridan,, J. M., Fu,, N., … Visvader,, J. E. (2013). Global changes in the mammary epigenome are induced by hormonal cues and coordinated by Ezh2. Cell Reports, 3(2), 411–426. https://doi.org/10.1016/j.celrep.2012.12.020
Palmeira,, P., Quinello,, C., Silveira‐Lessa,, A. L., Zago,, C. A., & Carneiro‐Sampaio,, M. (2012). IgG placental transfer in healthy and pathological pregnancies. Clinical and Developmental Immunology, 2012, 13. https://doi.org/10.1155/2012/985646
Pathania,, R., Ramachandran,, S., Elangovan,, S., Padia,, R., Yang,, P., Cinghu,, S., … Thangaraju,, M. (2015). DNMT1 is essential for mammary and cancer stem cell maintenance and tumorigenesis. Nature Communications, 6, 1–11. https://doi.org/10.1038/ncomms7910
Patki,, S., Kadam,, S., Chandra,, V., & Bhonde,, R. (2010). Human breast milk is a rich source of multipotent mesenchymal stem cells. Human Cell, 23(2), 35–40. https://doi.org/10.1111/j.1749-0774.2010.00083.x
Pellacani,, D., Bilenky,, M., Kannan,, N., Heravi‐Moussavi,, A., Knapp,, D. J. H. F., Gakkhar,, S., … Eaves,, C. J. (2016). Analysis of Normal human mammary epigenomes reveals cell‐specific active enhancer states and associated transcription factor networks. Cell Reports, 17(8), 2060–2074. https://doi.org/10.1016/j.celrep.2016.10.058
Peters,, J. (2014). The role of genomic imprinting in biology and disease: An expanding view. Nature Reviews Genetics, 15, 517–530. https://doi.org/10.1038/nrg3766
Ratajczak,, C. K., Herzog,, E. D., & Muglia,, L. J. (2010). Clock gene expression in gravid uterus and extra‐embryonic tissues during late gestation in the mouse. Reproduction, Fertility and Development, 22(5), 743–750. https://doi.org/10.1071/RD09243
Richter,, H. G., Hansell,, J. A., Raut,, S., & Giussani,, D. A. (2009). Melatonin improves placental efficiency and birth weight and increases the placental expression of antioxidant enzymes in undernourished pregnancy. Journal of Pineal Research, 46(4), 357–364. https://doi.org/10.1111/j.1600-079X.2009.00671.x
Rios,, A. C., Fu,, N. Y., Lindeman,, G. J., & Visvader,, J. E. (2014). In situ identification of bipotent stem cells in the mammary gland. Nature, 506(7488), 322–327. https://doi.org/10.1038/nature12948
Sánchez,, C. L., Cubero,, J., Sánchez,, J., Chanclón,, B., Rivero,, M., Rodríguez,, A. B., & Barriga,, C. (2009). The possible role of human milk nucleotides as sleep inducers. Nutritional Neuroscience, 12(1), 2–8. https://doi.org/10.1179/147683009X388922
Santos,, C. O., Dolzhenko,, E., Hodges,, E., Smith,, A. D., & Hannon,, G. J. (2015). An epigenetic memory of pregnancy in the mouse mammary gland. Cell Reports, 11(7), 1102–1109. https://doi.org/10.1016/j.celrep.2015.04.015.An
Savino,, F., & Liguori,, S. A. (2008). Update on breast milk hormones: Leptin, ghrelin and adiponectin. Clinical Nutrition, 27(1), 42–47. https://doi.org/10.1016/j.clnu.2007.06.006
Schaller,, F., Watrin,, F., Sturny,, R., Massacrier,, A., Szepetowski,, P., & Muscatelli,, F. (2010). A single postnatal injection of oxytocin rescues the lethal feeding behaviour in mouse newborns deficient for the imprinted Magel2 gene. Human Molecular Genetics, 19(24), 4895–4905. https://doi.org/10.1093/hmg/ddq424
Schröder,, H. J., & Power,, G. G. (1997). Engine and radiator: Fetal and placental interactions for heat dissipation. Experimental Physiology, 82(2), 403–414. https://doi.org/10.1113/expphysiol.1997.sp004035
Sekita,, Y., Wagatsuma,, H., Nakamura,, K., Ono,, R., Kagami,, M., Wakisaka,, N., … Ishino,, F. (2008). Role of retrotransposon‐derived imprinted gene, Rtl1, in the feto‐maternal interface of mouse placenta. Nature Genetics, 40(2), 243–248. https://doi.org/10.1038/ng.2007.51
Shackleton,, M., Vaillant,, F., Simpson,, K. J., Stingl,, J., Smyth,, G. K., Asselin‐Labat,, M. L., … Visvader,, J. E. (2006). Generation of a functional mammary gland from a single stem cell. Nature, 439(7072), 84–88. https://doi.org/10.1038/nature04372
Shehadeh,, N., Khaesh‐Goldberg,, E., Shamir,, R., Perlman,, R., Sujov,, P., Tamir,, A., & Makhoul,, I. R. (2003). Insulin in human milk: Postpartum changes and effect of gestational age. Archives of Disease in Childhood: Fetal and Neonatal Edition, 88(3), 214–216.
Sibley,, C. P., Glazier,, J. D., Greenwood,, S. L., Lacey,, H., Mynett,, K., Speake,, P., … Powell,, T. L. (2002). Regulation of placental transfer: The Na+/H+ exchanger—a review. Placenta, 23(Suppl. 1), S39–S46. https://doi.org/10.1053/plac.2002.0790
Spencer,, H. G., & Clark,, A. G. (2014). Non‐conflict theories for the evolution of genomic imprinting. Heredity, 113(2), 112–118. https://doi.org/10.1038/hdy.2013.129
Stringer,, J. M., Pask,, A. J., Shaw,, G., & Renfree,, M. B. (2014). Post‐natal imprinting: Evidence from marsupials. Heredity, 113(2), 145–155. https://doi.org/10.1038/hdy.2014.10
Stringer,, J. M., Suzuki,, S., Pask,, A. J., Shaw,, G., & Renfree,, M. B. (2012). Selected imprinting of INS in the marsupial. Epigenetics %26 Chromatin, 5(1), 14. https://doi.org/10.1186/1756-8935-5-14
Štulc,, J. (1997). Placental transfer of inorganic ions and water. Physiological Reviews, 77, 805–836. Retrieved from https://www.physiology.org/doi/abs/10.1152/physrev.1997.77.3.805
Teixeira da Rocha,, S., Charalambous,, M., Lin,, S. P., Gutteridge,, I., Ito,, Y., Gray,, D., … Ferguson‐Smith,, A. C. (2009). Gene dosage effects of the imprinted delta‐like homologue 1 (Dlk1/Pref1) in development: Implications for the evolution of imprinting. PLoS Genetics, 5(2), e1000392. https://doi.org/10.1371/journal.pgen.1000392
Tucci,, V., Isles,, A. R., Kelsey,, G., Ferguson‐Smith,, A. C., Bartolomei,, M. S., Benvenisty,, N., … Wilkins,, J. (2019, February 21). Genomic imprinting and physiological processes in mammals. Cell, 176(5), 952–965. https://doi.org/10.1016/j.cell.2019.01.043
Van De Perre,, P. (2003). Transfer of antibody via mother`s milk. Vaccine, 21(24), 3374–3376. https://doi.org/10.1016/S0264-410X(03)00336-0
Vaughan,, L. A., Weber,, C. W., & Kemberling,, S. R. (1979). Longitudinal changes in the mineral content of human milk. American Journal of Clinical Nutrition, 32(11), 2301–2306.
Victora,, C. G., Bahl,, R., Barros,, A. J. D., França,, G. V. A., Horton,, S., Krasevec,, J., … Richter,, L. (2016). Breastfeeding in the 21st century: Epidemiology, mechanisms, and lifelong effect. The Lancet, 387(10017), 475–490. https://doi.org/10.1016/S0140-6736(15)01024-7
Visvader,, J. E., & Stingl,, J. (2014). Mammary stem cells and the differentiation hierarchy: Current status and perspectives. Genes %26 Development, 28(11), 1143–1158. https://doi.org/10.1101/gad.242511.114.targeted
Waddell,, B. J., Wharfe,, M. D., Crew,, R. C., & Mark,, P. J. (2012). A rhythmic placenta? Circadian variation, clock genes and placental function. Placenta, 33(7), 533–539. https://doi.org/10.1016/j.placenta.2012.03.008
Watson,, C. J. (2006). Key stages in mammary gland development involution: Apoptosis and tissue remodelling that convert the mammary gland from milk factory to a quiescent organ. Breast Cancer Research, 8(2), 1–5. https://doi.org/10.1186/bcr1401
Weksberg,, R., Shen,, D. R., Fei,, Y. L., Song,, Q. L., & Squire,, J. (1993). Disruption of insulin‐like growth factor 2 imprinting in Beckwith‐Wiedemann syndrome. Nature Genetics, 5(2), 143–150.
Wells,, J. C. K. (2002). Thermal environment and human birth weight. Journal of Theoretical Biology, 214(3), 413–425. https://doi.org/10.1006/jtbi.2001.2465
Wharfe,, M. D., Mark,, P. J., & Waddell,, B. J. (2011). Circadian variation in placental and hepatic clock genes in rat pregnancy. Endocrinology, 152(9), 3552–3560. https://doi.org/10.1210/en.2011-0081
Witebsky,, E., Anderson,, G. W., & Heide,, A. (1942). Demonstration of Rh antibody in breast milk. Proceedings of the Society for Experimental Biology and Medicine, 49(2), 179–183. https://doi.org/10.3181/00379727-49-13506
Wolf,, J. B., & Hager,, R. (2006). A maternal‐offspring coadaptation theory for the evolution of genomic imprinting. PLoS Biology, 4(12), 2238–2243. https://doi.org/10.1371/journal.pbio.0040380
Yonekura,, S., Ohata,, M., Tsuchiya,, M., Tokita,, H., Mizusawa,, M., & Tokutake,, Y. (2019). Peg1/Mest, an imprinted gene, is involved in mammary gland maturation. Journal of Cellular Physiology, 234(2), 1080–1087. https://doi.org/10.1002/jcp.27219
Yu,, H., Dilbaz,, S., Coßmann,, J., Hoang,, A. C., Diedrich,, V., Herwig,, A., … Röszer,, T. (2019). Breast milk alkylglycerols sustain beige adipocytes through adipose tissue macrophages. Journal of Clinical Investigation, 129(6), 2485–2499. https://doi.org/10.1172/JCI125646
Zhou,, Q., Li,, M., Wang,, X., Li,, Q., Wang,, T., Zhu,, Q., … Li,, X. (2012). Immune‐related MicroRNAs are abundant in breast milk exosomes. International Journal of Biological Sciences, 8(1), 118–123.

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