Hostname: page-component-848d4c4894-tn8tq Total loading time: 0 Render date: 2024-06-18T20:46:42.446Z Has data issue: false hasContentIssue false

Epigenetics: a possible role in acute and transgenerational regulation of dairy cow milk production

Published online by Cambridge University Press:  19 December 2011

K. Singh*
Affiliation:
Growth and Lactation Team, Animal Productivity Group, AgResearch Ltd, Ruakura Research Centre, Private Bag 3123, Hamilton 3240, New Zealand
A. J. Molenaar
Affiliation:
Growth and Lactation Team, Animal Productivity Group, AgResearch Ltd, Ruakura Research Centre, Private Bag 3123, Hamilton 3240, New Zealand
K. M. Swanson
Affiliation:
Growth and Lactation Team, Animal Productivity Group, AgResearch Ltd, Ruakura Research Centre, Private Bag 3123, Hamilton 3240, New Zealand
B. Gudex
Affiliation:
Livestock Improvement Corporation, Hamilton, New Zealand
J. A. Arias
Affiliation:
Livestock Improvement Corporation, Hamilton, New Zealand
R. A. Erdman
Affiliation:
Department of Animal and Avian Sciences, University of Maryland, College Park, MD 20742, USA
K. Stelwagen
Affiliation:
SciLactis Ltd, Waikato Innovation Park, Ruakura Road, Hamilton 3240, New Zealand
Get access

Abstract

A potential role for epigenetic mechanisms in the regulation of mammary function in the dairy cow is emerging. Epigenetics is the study of heritable changes in genome function that occur because of chemical changes rather than DNA sequence changes. DNA methylation is an epigenetic event that results in the silencing of gene expression and may be passed on to the next generation. However, recent studies investigating different physiological states and changes in milk protein gene expression suggest that DNA methylation may also play an acute, regulatory, role in gene transcription. This overview will highlight the role of DNA methylation in the silencing of milk protein gene expression during mastitis and mammary involution. Moreover, environmental factors such as nutrition may induce epigenetic modifications of gene expression. The current research investigating the possibility of in utero, hence cross-generational, epigenetic modifications in dairy cows will also be discussed. Understanding how the mammary gland responds to environmental cues provides a potential to enhance milk production not only of the dairy cow but also of her daughter.

Type
Full Paper
Copyright
Copyright © The Animal Consortium 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Akers, RM, Keys, JE 1985. Effect of suckling intensity on human growth hormone binding, biochemical composition, and histological characteristics of ovine mammary glands. Domestic Animal Endocrinology 2, 159172.Google Scholar
Barker, DJP 1995. Fetal origins of coronary heart disease. British Medical Journal 311, 171174.CrossRefGoogle ScholarPubMed
Barker, DJP, Gluckman, PD, Godfrey, KM, Harding, JE, Owens, JA, Robinson, JS 1993. Fetal nutrition and cardiovascular disease in adult life. Lancet 341, 938941.Google Scholar
Bartel, DP 2009. MicroRNAs: target recognition and regulatory functions. Cell 136, 215233.CrossRefGoogle ScholarPubMed
Berry, DP, Lonergan, P, Butler, ST, Cromie, AR, Fair, T, Mossa, F, Evans, AC 2008. Negative influence of high maternal milk production before and after conception on offspring survival and milk production in dairy cattle. Journal of Dairy Science 91, 329337.CrossRefGoogle ScholarPubMed
Bird, A 2002. DNA methylation patterns and epigenetic memory. Genes and Development 16, 621.Google Scholar
Bird, AP, Wolffe, AP 1999. Methylation-induced repression-belts, braces, and chromatin. Cell 5, 451454.CrossRefGoogle Scholar
Bormann, J, Wiggans, GR, Druet, T, Gengler, N 2003. Within-herd effects of age at test day and lactation stage on test-day yields. Journal of Dairy Science 86, 37653774.CrossRefGoogle ScholarPubMed
Capuco, AV, Akers, RM, Smith, JJ 1997. Mammary growth in Holstein cows during the dry period: quantification of nucleic acids and histology. Journal of Dairy Science 80, 477487.CrossRefGoogle ScholarPubMed
Capuco, AV, Wood, DL, Baldwin, R, Mcleod, K, Paape, MJ 2001. Mammary cell number, proliferation, and apoptosis during a bovine lactation: relation to milk production and effect of bST. Journal of Dairy Science 84, 21772187.CrossRefGoogle ScholarPubMed
Choi, YJ, Jang, K, Yim, DS, Baik, MG, Myung, KH, Kim, YS, Lee, HJ, Kim, JS, Han, IK 1998. Effects of compensatory growth on the expression of milk protein gene and biochemical changes of the mammary gland in Holstein cows. The Journal of Nutritional Biochemistry 9, 380387.Google Scholar
Clarkson, RW, Wayland, MT, Lee, J, Freeman, T, Watson, CJ 2004. Gene expression profiling of mammary gland development reveals putative roles for death receptors and immune mediators in post-lactational regression. Breast Cancer Research 6, R92R108.CrossRefGoogle ScholarPubMed
Connor, EE, Siferd, S, Elsasser, TH, Evock-Clover, CM, Van Tassell, CP, Sonstegard, TS, Fernandes, VM, Capuco, AV 2008. Effect of increased milking frequency on gene expression in the bovine mammary gland. BioMed Central Genomics 9, 362.Google ScholarPubMed
Cooper, CV, Stelwagen, K, Singh, K, Farr, VC, Prosser, CG, Davis, SR 2004. Expression of the tight junction protein zonula occludens-1 during mammary engorgement. Proceedings of the New Zealand Society of Animal Production 64, 4347.Google Scholar
Cropley, JE, Suter, CM, Beckman, KB, Martin, DIK 2006. Germ-line epigenetic modification of the murine Avy allele by nutritional supplementation. Proceedings of the National Academy of Sciences of the United States of America 103, 1730817312.CrossRefGoogle Scholar
Dalley, DE, Davis, SR 2006. Effect of an extended milking interval on recovery of milk yield and somatic cell count in dairy cows. Proceedings of the New Zealand Society of Animal Production 66, 241244.Google Scholar
Dean, W, Santos, F, Reik, W 2003. Epigenetic reprogramming in early mammalian development and following somatic nuclear transfer. Seminars in Cell and Developmental Biology 14, 93100.CrossRefGoogle ScholarPubMed
Duhl, DM, Vrieling, H, Miller, KA, Wolff, GL, Barsh, GS 1994. Neomorphic agouti mutations in obese yellow mice. Nature Genetics 8, 5965.Google Scholar
Feng, Z, Marti, A, Jehn, B, Altermatt, HJ, Chicaiza, G, Jaggi, R 1995. Glucocorticoid and progesterone inhibit involution and programmed cell death in the mouse mammary gland. The Journal of Cell Biology 131, 10951103.CrossRefGoogle ScholarPubMed
Finucane, KA, McFadden, TB, Bond, JP, Kennelly, JJ, Zhao, FQ 2008. Onset of lactation in the bovine mammary gland: gene expression profiling indicates a strong inhibition of gene expression in cell proliferation. Functional and Integrative Genomics 8, 251264.CrossRefGoogle Scholar
Ford, JA Jr, Park, CS 2001. Nutritionally directed compensatory growth enhances heifer development and lactation potential. Journal of Dairy Science 84, 16691678.CrossRefGoogle ScholarPubMed
Gilmore, AP, Metcalfe, AD, Romer, LH, Streuli, CH 2000. Integrin-mediated survival signals regulate the apoptotic function of Bax through its conformation and subcellular localization. The Journal of Cell Biology 149, 431446.CrossRefGoogle ScholarPubMed
Hamann, J, Reichmuth, J 1990. Compensatory milk production within the bovine udder: effects of short-term non-milking of single quarters. Journal of Dairy Research 57, 1722.CrossRefGoogle ScholarPubMed
Holst, BD, Hurley, WL, Nelson, DR 1987. Involution of the bovine mammary gland: histological and ultrastructural changes. Journal of Dairy Science 70, 935944.Google Scholar
Jaenisch, R, Bird, A 2003. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nature Genetics 33, 245254.CrossRefGoogle ScholarPubMed
Jaggi, R, Marti, A, Guo, K, Feng, Z, Friis, RR 1996. Regulation of a physiological apoptosis: mouse mammary involution. Journal of Dairy Science 79, 10741084.CrossRefGoogle ScholarPubMed
Jirtle, RL, Skinner, MK 2007. Environmental epigenomics and disease susceptibility. Nature Reviews Genetics 8, 253262.Google Scholar
Johnson, ML, Levy, J, Supowit, SC, Yu-Lee, LY, Rosen, JM 1983. Tissue and cell-specific casein gene expression. II. Relationship to site-specific DNA methylation. The Journal of Biological Chemistry 258, 1080510811.Google Scholar
Jones, PA, Takai, D 2001. The role of DNA methylation in mammalian epigenetics. Science 293, 10681070.CrossRefGoogle ScholarPubMed
Kangaspeska, S, Stride, B, Métivier, R, Polycarpou-Schwarz, M, Ibberson, D, Carmouche, RP, Benes, V, Gannon, F, Reid, G 2008. Transient cyclical methylation of promoter DNA. Nature 452, 112115.CrossRefGoogle ScholarPubMed
Klose, RJ, Bird, AP 2006. Genomic DNA methylation: the mark and its mediators. Trends in Biochemical Sciences 31, 8997.CrossRefGoogle ScholarPubMed
Laible, G, Brophy, B, Knighton, D, Wells, DN 2007. Compositional analysis of dairy products derived from clones and cloned transgenic cattle. Theriogenology 67, 166177.CrossRefGoogle ScholarPubMed
Li, M, Liu, X, Robinson, G, Bar-Peled, U, Wagner, KU, Young, WS, Hennighausen, L, Furth, PA 1997. Mammary-derived signals activate programmed cell death during the first stage of mammary gland involution. Proceedings of the National Academy of Sciences of the United States of America 94, 34253430.CrossRefGoogle ScholarPubMed
Lumey, LH 1992. Decreased birthweights in infants after maternal in utero exposure to the Dutch famine of 1944–1945. Paediatric and Perinatal Epidemiology 6, 240253.CrossRefGoogle Scholar
Lumey, LH, Stein, AD, Ravelli, ACJ 1995. Timing of prenatal starvation in women and birth weight in their first and second born offspring: the Dutch Famine Birth Cohort study. European Journal of Obstetrics & Gynecology and Reproductive Biology 61, 2330.Google Scholar
Master, SR, Hartman, JL, D'Cruz, CM, Moody, SE, Keiper, EA, Ha, SI, Cox, JD, Belka, GK, Chodosh, LA 2002. Functional microarray analysis of mammary organogenesis reveals a developmental role in adaptive thermogenesis. Journal of Molecular Endocrinology 16, 11851203.Google Scholar
McMahon, CD, Farr, VC, Singh, K, Wheeler, TT, Davis, SR 2004. Decreased expression of beta1-integrin and focal adhesion kinase in epithelial cells may initiate involution of mammary glands. Journal of Cellular Physiology 200, 318325.CrossRefGoogle ScholarPubMed
Métivier, R, Gallais, R, Tiffoche, C, Le Péron, C, Jurkowska, RZ, Carmouche, RP, Ibberson, D, Barath, P, Demay, F, Reid, G, Benes, V, Jeltsch, A, Gannon, F, Salbert, G 2008. Cyclical DNA methylation of a transcriptionally active promoter. Nature 452, 4550.CrossRefGoogle ScholarPubMed
Molenaar, AJ, Davis, SR, Wilkins, RJ 1992. Expression of alpha-lactalbumin, alpha-s1 casein, and lactoferrin genes is heterogeneous in sheep and cattle mammary tissue. The Journal of Histochemistry and Cytochemistry 40, 611618.CrossRefGoogle Scholar
Molenaar, AJ, Kuys, YM, Davis, SR, Wilkins, RJ, Mead, PE, Tweedie, JW 1996. Elevation of lactoferrin gene expression in developing, ductal, resting, and regressing parenchymal epithelium of the ruminant mammary gland. Journal of Dairy Science 79, 11981208.Google Scholar
Molenaar, A, Seyfert, HM, Murney, R, Biet, J, Erdman, R, Oden, K, Henderson, H, Rijnkels, M, Stelwagen, K, Singh, K 2010. Compaction of the alpha-S1-casein and opening of a defensin promoter occurs during S. uberis infection of the bovine mammary gland and after cessation of milking, the casein promoter begins to close up after 24 hours. Conference at the 7th Annual International Symposium: Milk Genomics and Human Health, UC Davis, CA, USA. Retrieved February 20, 2011 from http://milkgenomics.org/symposia/2010-symposium/2010-posters/Molenaar%20IMGC%20poster%202010.pdf/viewGoogle Scholar
Moore, T, Reik, W 1996. Genetic conflict in early development: parental imprinting in normal and abnormal growth. Reviews of Reproduction 1, 7377.CrossRefGoogle ScholarPubMed
Morgan, DK, Whitelaw, E 2008. The case for transgenerational epigenetic inheritance in humans. Mammalian Genome 19, 394397.Google Scholar
Morgan, HD, Sutherland, HE, Martin, DIK, Whitelaw, E 1999. Epigenetic inheritance at the agouti locus in the mouse. Nature Genetics 23, 314318.CrossRefGoogle ScholarPubMed
Noble, MS, Hurley, WL 1999. Effects of secretion removal on bovine mammary gland function following an extended milk stasis. Journal of Dairy Science 82, 17231730.CrossRefGoogle ScholarPubMed
Park, CS 2005. Role of compensatory mammary growth in epigenetic control of gene expression. The Journal of the Federation of American Societies for Experimental Biology 19, 15861591.CrossRefGoogle ScholarPubMed
Park, CS, Baik, MG, Keller, WL, Berg, IE, Erickson, GM 1989. Role of compensatory growth in lactation: a stair-step nutrient regimen modulates differentiation and lactation of bovine mammary gland. Growth, Development, and Aging 53, 159166.Google Scholar
Platenburg, GJ, Vollebregt, EJ, Karatzas, CN, Kootwijk, EP, de Boer, HA, Strijker, R 1996. Mammary gland-specific hypomethylation of Hpa II sites flanking the bovine alpha S1-casein gene. Transgenic Research 5, 421431.CrossRefGoogle ScholarPubMed
Pryce, JE, Harris, BL 2006. Genetics of body condition score in New Zealand dairy cows. Journal of Dairy Science 89, 44244432.Google Scholar
Ramsahoye, BH, Biniszkiewicz, D, Lyko, F, Clark, V, Bird, AP, Jaenisch, R 2000. Non-CpG methylation is prevalent in embryonic stem cells and may be mediated by DNA methyltransferase 3a. Proceedings of the National Academy of Sciences of the United States of America 97, 52375242.CrossRefGoogle ScholarPubMed
Reik, W, Walter, J 2001. Genomic imprinting: parental influence on the genome. Nature Reviews Genetics 2, 2132.Google Scholar
Riggs, AD, Martienssen, RA, Russo, VEA 1996. Introduction. In Epigenetic mechanisms of gene regulation (ed. VEA Russo, RA Martienssen and AD Riggs), volume 32, pp. 14. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, USA.Google Scholar
Rijnkels, M, Kabotyanski, E, Montazer-Torbati, MB, Beauvais, CH, Vassetzky, Y, Rosen, JM, Devinoy, E 2010. The epigenetic landscape of mammary development and functional differentiation. Journal of Mammary Gland Biology and Neoplasia 15, 85100.CrossRefGoogle ScholarPubMed
Roche, JR, Lee, JM, Berry, DP 2006. Pre-conception energy balance and secondary sex ratio-partial support for the Trivers–Willard hypothesis in dairy cows. Journal of Dairy Science 89, 21192125.CrossRefGoogle ScholarPubMed
Ruvinsky, A 1999. Basics of gametic imprinting. Journal of Animal Science 77, 228237.CrossRefGoogle ScholarPubMed
Sejrsen, K, Huber, JT, Tucker, HA, Akers, RM 1982. Influence of nutrition of mammary development in pre- and postpubertal heifers. Journal of Dairy Science 65, 793800.Google Scholar
Singh, K, Swanson, K, Couldrey, C, Seyfert, H-M, Stelwagen, K 2009a. DNA methylation events associated with the suppression of milk protein gene expression during involution of the bovine mammary gland. Proceedings of the New Zealand Society of Animal Production 69, 5759.Google Scholar
Singh, K, Vetharaniam, I, Prewitz, M, Dobson, J, Stelwagen, K 2009b. Understanding the interaction of prolactin and leukaemia inhibitory growth factor signalling during the switch from lactation to involution. Proceedings of the New Zealand Society of Animal Production 69, 6567.Google Scholar
Singh, K, Erdman, RA, Swanson, KM, Molenaar, AJ, Maqbool, NJ, Wheeler, TT, Arias, JA, Quinn-Walsh, EC, Stelwagen, K 2010a. Epigenetic regulation of milk production in dairy cows. Journal of Mammary Gland Biology and Neoplasia 15, 101112.CrossRefGoogle ScholarPubMed
Singh, K, Molenaar, AJ, Swanson, KM, Stelwagen, K 2010b. DNA methylation is associated with a suppression of αS1-casein gene expression during involution and infection of the bovine mammary gland. Conference at the IDF World Dairy Summit, 8–11 November 2010, Auckland, New Zealand.Google Scholar
Singh, K, Dobson, J, Phyn, CVC, Davis, SR, Farr, VC, Molenaar, AJ, Stelwagen, K 2005. Milk accumulation decreases expression of genes involved in cell–extracellular matrix communication and is associated with induction of apoptosis in the bovine mammary gland. Livestock Production Science 98, 6778.CrossRefGoogle Scholar
Singh, K, Dobson, J, Oden, K, Molenaar, A, Murney, R, Swanson, K, Stelwagen, K 2011. Regulation of STAT and IGF signalling during reversible and irreversible involution of the bovine mammary gland. Journal of Dairy Science 94 (E-suppl. 1), 751.Google Scholar
Singh, K, Davis, SR, Dobson, JM, Molenaar, AJ, Wheeler, TT, Prosser, CG, Farr, VC, Oden, K, Swanson, KM, Phyn, CV, Hyndman, DL, Wilson, T, Henderson, HV, Stelwagen, K 2008. cDNA microarray analysis reveals antioxidant and immune genes are up-regulated during involution of the bovine mammary gland. Journal of Dairy Science 91, 22362246.CrossRefGoogle Scholar
Stein, T, Morris, JS, Davies, CR, Weber-Hall, SJ, Duffy, MA, Heath, VJ, Bell, AK, Ferrier, RK, Sandilands, GP, Gusterson, BA 2004. Involution of the mouse mammary gland is associated with an immune cascade and an acute-phase response, involving LBP, CD14 and STAT3. Breast Cancer Research 6, R75R91.CrossRefGoogle Scholar
Stelwagen, K 2001. Effect of milking frequency on mammary functioning and shape of the lactation curve. Journal of Dairy Science 84, E204E211.Google Scholar
Stelwagen, K, Farr, VC, Nicholas, GD, Davis, SR, Prosser, CG 2008. Effect of milking interval on milk yield and quality and the rate of recovery during subsequent frequent milking. Livestock Science 114, 176180.Google Scholar
Strahl, BD, Allis, CD 2000. The language of covalent histone modifications. Nature 403, 4145.Google Scholar
Suchyta, SP, Sipkovsky, S, Halgren, RG, Kruska, R, Elftman, M, Weber-Nielsen, M, Vandehaar, MJ, Xiao, L, Tempelman, RJ, Coussens, PM 2003. Bovine mammary gene expression profiling using a cDNA microarray enhanced for mammary-specific transcripts. Physiological Genomics 16, 818.Google Scholar
Swanson, KM, Stelwagen, K, Erdman, RA, Singh, K 2011. Acute DNA methylation changes are associated with involution and re-initiation of lactation in dairy cows. Journal of Dairy Science 94 (E-suppl. 1), 433.Google Scholar
Swanson, KM, Stelwagen, K, Dobson, J, Henderson, HV, Davis, SR, Farr, VC, Singh, K 2009. Transcriptome profiling of Streptococcus uberis-induced mastitis reveals fundamental differences between immune gene expression in the mammary gland and in a primary cell culture model. Journal of Dairy Science 92, 117129.Google Scholar
Thompson, MD, Nakhasi, HL 1985. Methylation and expression of rat kappa-casein gene in normal and neoplastic rat mammary gland. Cancer Research 45, 12911295.Google ScholarPubMed
Vanselow, J, Yang, W, Herrmann, J, Zerbe, H, Schuberth, HJ, Petzl, W, Tomek, W, Seyfert, HM 2006. DNA-remethylation around a STAT5-binding enhancer in the far distal alphaS1-casein promoter is associated with abrupt shut-down of alphaS1-casein synthesis during acute mastitis. Journal of Molecular Endocrinology 37, 463477.Google Scholar
Van Tassell, CP, Wiggans, GR, VanRaden, PM, Norman, HD 1997. Changes in USDA-DHIA genetic evaluations. Animal Improvement Programs Laboratory Research Report CH9 (8-97). US Department of Agriculture/Agricultural Research Service, Washington, DC, USA.Google Scholar
Vasicek, TJ, Zeng, L, Guan, XJ, Zhang, T, Costantini, F, Tilghman, SM 1997. Two dominant mutations in the mouse fused gene are the result of transposon insertions. Genetics 147, 777786.CrossRefGoogle ScholarPubMed
Waterland, RA, Jirtle, RL 2003. Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Molecular and Cellular Biology 23, 52935300.CrossRefGoogle ScholarPubMed
Waterland, RA, Travisano, M, Tahiliani, KG 2007. Diet-induced hypermethylation at agouti viable yellow is not inherited transgenerationally through the female. The Journal of the Federation of American Societies for Experimental Biology 21, 33803385.Google Scholar
Wheelock, JV, Rook, JAF, Dodd, FH 1965. The effect of incomplete milking or of an extended milking interval on the yield and composition of cow's milk. Journal of Dairy Research 32, 237248.Google Scholar
Wilde, CJ, Addey, CV, Li, P, Fernig, DG 1997. Programmed cell death in bovine mammary tissue during lactation and involution. Experimental Physiology 82, 943953.CrossRefGoogle ScholarPubMed
Wolff, GL, Kodell, RL, Moore, SR, Cooney, CA 1998. Maternal epigenetics and methyl supplements affect agouti gene expression in Avy/a mice. The Journal of the Federation of American Societies for Experimental Biology 12, 949957.Google Scholar
Zeng, L, Fagotto, F, Zhang, T, Hsu, W, Vasicek, TJ, Perry, WL, Lee, JJ, Tilghman, SM, Gumbiner, BM, Costantini, F 1997. The mouse fused locus encodes Axin, an inhibitor of the Wnt signalling pathway that regulates embryonic axis formation. Cell 90, 181192.CrossRefGoogle ScholarPubMed