Skip to main content
SpringerLink
Log in

Molecular-Genetic Bases of Mammary Gland Development Using the Example of Cattle and Other Animal Species: I. Embryonic and Pubertal Developmental Stage

  • Published:
Russian Journal of Genetics Aims and scope Submit manuscript

Abstract

The growing demand of society for the products of farm animals entails continuous modernization of breeding programs. In order to improve the accuracy of genomic assessment of breeding value, the models that allow applying the data on contributions of specific polymorphic loci to the formation of economically beneficial traits have been used recently. Taking into account the functional role of the genes responsible for the formation of the mammary gland is important to improve the reliability of prediction for milk yield. This review describes the molecular-genetic basis of mammary gland development at the embryonic, prepubertal, and pubertal stages of development using the example of cattle and some other mammals. Particular focus is on epigenetic regulation. The data on genetics, morphophysiology, endocrinology, and the effects of microorganisms at different stages of mammary gland development are presented.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.

Similar content being viewed by others

REFERENCES

  1. FAO, Food Outlook—Biannual Report on Global Food Markets, Rome, 2021. https://doi.org/10.4060/cb7491en

  2. FAO, Food Outlook—Biannual Report on Global Food Markets, Rome, 2010. http://www.fao.org/3/a-ak349e.pdf. Accessed November 20, 2021.

  3. Hayes, B. and Goddard, M., Genome-wide association and genomic selection in animal breeding, Genome, 2010, vol. 53, no. 11, pp. 876—883. https://doi.org/10.1139/G10-076

    Article  CAS  PubMed  Google Scholar 

  4. Stolpovsky, Y.A., Piskunov, A.K., and Svishcheva, G.R., Genomic selection: I. Latest trends and possible ways of development, Russ. J. Genet., 2020, vol. 56, no. 9, pp. 1044—1054. https://doi.org/10.1134/S1022795420090148

    Article  CAS  Google Scholar 

  5. De Roos, A.P.W., Hayes, B.J., and Goddard, M.E., Reliability of genomic predictions across multiple populations, Genetics, 2009, vol. 183, no. 4, pp. 1545—1553. https://doi.org/10.1534/genetics.109.104935

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Edwards, S.M., Sørensen, I.F., Sarup, P., et al., Genomic prediction for quantitative traits is improved by mapping variants to gene ontology categories in Drosophila melanogaster, Genetics, 2016, vol. 203, no. 4, pp. 1871—1883. https://doi.org/10.1534/genetics.116.187161

    Article  PubMed  PubMed Central  Google Scholar 

  7. Mollandin, F., Gilbert, H., Croiseau, P., and Rau, A., Accounting for overlapping annotations in genomic prediction models of complex traits, Res. Square, 2022. https://doi.org/10.21203/rs.3.rs-1366477/v1.

  8. Strucken, E.M., Laurenson, Y.C.S.M., and Brockmann, G.A., Go with the flow–biology and genetics of the lactation cycle, Front. Genet., 2015, vol. 6, p. 118. https://doi.org/10.3389/fgene.2015.00118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Finot, L., Chanat, E., and Dessauge, F., Bovine mammary gland development: new insights into the epithelial hierarchy, bioRxiv, 2018, p. 251637. https://doi.org/10.1101/251637

  10. Van Raden, P.M., Symposium review: how to implement genomic selection, J. Dairy Sci., 2020, vol. 103, no. 6, pp. 5291—5301. https://doi.org/10.3168/jds.2019-17684

    Article  CAS  Google Scholar 

  11. Ibeagha-Awemu, E.M. and Zhao, X., Epigenetic marks: regulators of livestock phenotypes and conceivable sources of missing variation in livestock improvement programs, Front. Genet., 2015, vol. 6, p. 302. https://doi.org/10.3389/fgene.2015.00302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Feinberg, A.P., Irizarry, R.A., and Fradin, D., Personalized epigenomic signatures that are stable over time and covary with body mass index, Sci. Transl. Med., 2010, vol. 2, no. 49, pp. 49—67. https://doi.org/10.1126/scitranslmed.3001262

    Article  CAS  Google Scholar 

  13. Yang, Z., Liu, S., Hu, Y., et al., Comparative whole genome DNA methylation profiling of cattle tissues reveals global and tissue-specific methylation patterns, BMC Biol., 2020, vol. 18, no. 85, pp. 1—17. https://doi.org/10.1186/s12915-020-00793-5

    Article  CAS  Google Scholar 

  14. Su, J., Wang, Y., Xing, X., et al., Genome-wide analysis of DNA methylation in bovine placentas, BMC Genomics, 2014, vol. 15, no. 12, pp. 1—11. https://doi.org/10.1186/1471-2164-15-12

    Article  Google Scholar 

  15. Park, S., Min, S., Choi, H.S., and Yoon, S., Deep recurrent neural network-based identification of precursor microRNAs, Adv. Neural Inf. Proc. Syst., 2017, vol. 30, pp. 1—10.

    CAS  Google Scholar 

  16. Liang, M., Li, Z., Chen, T., and Zeng, J., Integrative data analysis of multi-platform cancer data with a multimodal deep learning approach, IEEE/ACM Trans. Comput. Biol. Bioinf., 2014, vol. 12, no. 4, pp. 928—937. https://doi.org/10.1109/TCBB.2014.2377729

    Article  Google Scholar 

  17. Hilton, I.B., D’Ippolito, A.M., Vockley, C.M., et al., Epigenome editing by a CRISPR-Cas9-based acetyltransferase activates genes from promoters and enhancers, Nat. Biotechnol., 2015, vol. 33, no. 5, pp. 510—517. https://doi.org/10.1038/nbt.3199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Neville, M.C., McFadden, T.B., and Forsyth, I., Hormonal regulation of mammary differentiation and milk secretion, J. Mammary Gland Biol. Neoplasia, 2002, vol. 7, no. 1, pp. 49—66. https://doi.org/10.1023/A:1015770423167

    Article  PubMed  Google Scholar 

  19. Monteiro, F.L., Direito, I., and Helguero, L.A., Hormone signaling pathways in the postnatal mammary gland, in Tissue-Specific Cell Signaling, Cham: Springer-Verlag, 2020, pp. 279—315. https://doi.org/10.1007/978-3-030-44436-5_10

    Book  Google Scholar 

  20. VanHouten, J., Dann, P., McGeoch, G., et al., The calcium-sensing receptor regulates mammary gland parathyroid hormone–related protein production and calcium transport, J. Clin. Invest., 2004, vol. 113, no. 4, pp. 598—608. https://doi.org/10.1172/JCI18776

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Svennersten-Sjaunja, K. and Olsson, K., Endocrinology of milk production, Domest. Anim. Endocrinol., 2005, vol. 29, no. 2, pp. 241—258. https://doi.org/10.1016/j.domaniend.2005.03.006

    Article  CAS  PubMed  Google Scholar 

  22. Scully, K.M., Gleiberman, A.S., Lindzey, J., et al., Role of estrogen receptor-α in the anterior pituitary gland, Mol. Endocrinol., 1997, vol. 11, no. 6, pp. 674—681. https://doi.org/10.1210/mend.11.6.0019

    Article  CAS  PubMed  Google Scholar 

  23. Bachelot, A. and Binart, N., Reproductive role of prolactin, Reproduction, 2007, vol. 133, no. 2, pp. 361—369. https://doi.org/10.1530/REP-06-0299

    Article  CAS  PubMed  Google Scholar 

  24. Frasor, J. and Gibori, G., Prolactin regulation of estrogen receptor expression, Trends Endocrinol. Metab., 2003, vol. 14, no. 3, pp. 118—123. https://doi.org/10.1016/S1043-2760(03)00030-4

    Article  CAS  PubMed  Google Scholar 

  25. Banta, J.A. and Richards, C.L., Quantitative epigenetics and evolution, Heredity, 2018, vol. 121, no. 3, pp. 210—224. https://doi.org/10.1038/s41437-018-0114-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Holliday, R. and Pugh, J.E., DNA modification mechanisms and gene activity during development: developmental clocks may depend on the enzymic modification of specific bases in repeated DNA sequences, Science, 1975, vol. 187, no. 4173, pp. 226—232. https://doi.org/10.1126/science.187.4173.226

    Article  CAS  PubMed  Google Scholar 

  27. Chen, C., Yang, M.C.K., and Yang, T.P., Evidence that silencing of the HPRT promoter by DNA methylation is mediated by critical CpG sites, J. Biol. Chem., 2001, vol. 276, no. 1, pp. 320—328. https://doi.org/10.1074/jbc.M007096200

    Article  CAS  PubMed  Google Scholar 

  28. Laurent, L., Wong, E., Li, G., et al., Dynamic changes in the human methylome during differentiation, Genome Res., 2010, vol. 20, no. 3, pp. 320—331. https://doi.org/10.1101/gr.101907.109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Ivanova, E., Guillou, S.L., Hue-Beauvais, C., and Provost, F.L., Epigenetics: new insights into mammary gland biology, Genes, 2021, vol. 12, no. 2, p. 231. https://doi.org/10.3390/genes12020231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Choi, S.W. and Friso, S., Epigenetics: a new bridge between nutrition and health, Adv. Nutr., 2010, vol. 1, no. 1, pp. 8—16. https://doi.org/10.3945/an.110.1004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Jang, H. and Serra, C., Nutrition, epigenetics, and diseases, Clin. Nutr. Res., 2014, vol. 3, no. 1, pp. 1—8. https://doi.org/10.7762/cnr.2014.3.1.1

    Article  PubMed  PubMed Central  Google Scholar 

  32. Halušková, J., Holečková, B., and Staničová, J., DNA methylation studies in cattle, J. Appl. Genet., 2021, vol. 62, no. 1, pp. 121—136. https://doi.org/10.1007/s13353-020-00604-1

    Article  CAS  PubMed  Google Scholar 

  33. Karlić, R., Chung, H.R., Lasserre, J., et al., Histone modification levels are predictive for gene expression, Proc. Natl. Acad. Sci. U.S.A., 2010, vol. 107, no. 7, pp. 2926—2931. https://doi.org/10.1073/pnas.0909344107

    Article  PubMed  PubMed Central  Google Scholar 

  34. Shilatifard, A., Chromatin modifications by methylation and ubiquitination: implications in the regulation of gene expression, Annu. Rev. Biochem., 2006, vol. 75, pp. 243—269. https://doi.org/10.1146/annurev.biochem.75.103004.142422

    Article  CAS  PubMed  Google Scholar 

  35. Sparmann, A. and van Lohuizen, M., Polycomb silencers control cell fate, development and cancer, Nat. Rev. Cancer, 2006, vol. 6, no. 11, pp. 846—856. https://doi.org/10.1038/nrc1991

    Article  CAS  PubMed  Google Scholar 

  36. Silva, L.G., Ferguson, B.S., Avila, A.S., and Faciola, A.P., Sodium propionate and sodium butyrate effects on histone deacetylase (HDAC) activity, histone acetylation, and inflammatory gene expression in bovine mammary epithelial cells, J. Anim. Sci., 2018, vol. 96, no. 12, pp. 5244—5252. https://doi.org/10.1093/jas/sky373

    Article  PubMed  PubMed Central  Google Scholar 

  37. Moran, Y., Agron, M., Praher, D., and Technau, U., The evolutionary origin of plant and animal microRNAs, Nat. Ecol. Evol., 2017, vol. 1, no. 27, pp. 1—8. https://doi.org/10.1038/s41559-016-002

    Article  Google Scholar 

  38. Do, D.N. and Ibeagha-Awemu, E.M., Non-coding RNA roles in ruminant mammary gland development and lactation, Curr. Top. Lactation, 2017, vol. 55. https://doi.org/10.5772/67194

  39. Silveri, L., Tilly, G., Vilotte, J.L., and Provost, F.L., MicroRNA involvement in mammary gland development and breast cancer, Reprod. Nutr. Dev., 2006, vol. 46, no. 5, pp. 549—556. https://doi.org/10.1051/rnd:2006026

    Article  CAS  PubMed  Google Scholar 

  40. Wang, X., Gu, Z., and Jiang, H., MicroRNAs in farm animals, Animal, 2013, vol. 7, no. 10, pp. 1567—1575. https://doi.org/10.1017/S1751731113001183

    Article  CAS  PubMed  Google Scholar 

  41. Filipowicz, W., Bhattacharyya, S.N., and Sonenberg, N., Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight?, Nat. Rev. Genet., 2008, vol. 9, no. 2, pp. 102—114. https://doi.org/10.1038/nrg2290

    Article  CAS  PubMed  Google Scholar 

  42. Bartel, D.P., MicroRNAs: genomics, biogenesis, mechanism, and function, Cell, 2004, vol. 116, no. 2, pp. 281—297. https://doi.org/10.1016/S0092-8674(04)00045-5

    Article  CAS  PubMed  Google Scholar 

  43. Jiao, P., Yuan, Y., Zhang, M., et al., PRL/microRNA-183/IRS1 pathway regulates milk fat metabolism in cow mammary epithelial cells, Genes, 2020, vol. 11, no. 2, p. 196. https://doi.org/10.3390/genes11020196

    Article  CAS  PubMed Central  Google Scholar 

  44. Li, H.M., Wang, C.M., Li, Q.Z., and Li, X.J., MiR-15a decreases bovine mammary epithelial cell viability and lactation and regulates growth hormone receptor expression, Molecules, 2012, vol. 17, no. 10, pp. 12037—12048. https://doi.org/10.3390/molecules171012037

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Sakamoto, K., Komatsu, T., Kobayashi, T., et al., Growth hormone acts on the synthesis and secretion of α-casein in bovine mammary epithelial cells, J. Dairy Res., 2005, vol. 72, no. 3, pp. 264—270. https://doi.org/10.1017/S0022029905000889

    Article  CAS  PubMed  Google Scholar 

  46. Bian, Y., Lei, Y., Wang, C., et al., Epigenetic regulation of miR-29s affects the lactation activity of dairy cow mammary epithelial cells, J. Cell. Physiol., 2015, vol. 230, no. 9, pp. 2152—2163. https://doi.org/10.1002/jcp.24944

    Article  CAS  PubMed  Google Scholar 

  47. Wang, M., Moisá, S., Khan, M.J., et al., MicroRNA expression patterns in the bovine mammary gland are affected by stage of lactation, J. Dairy Sci., 2012, vol. 95, no. 11, pp. 6529—6535. https://doi.org/10.3168/jds.2012-5748

    Article  CAS  PubMed  Google Scholar 

  48. Kozomara, A., Birgaoanu, M., and Griffiths-Jones, S., miRBase: from microRNA sequences to function, Nucleic Acids Res., 2019, vol. 47, no. D1, pp. D155—D162. https://doi.org/10.1093/nar/gky1141

    Article  CAS  PubMed  Google Scholar 

  49. Dysin, A.P., Barkova, O.Y., and Pozovnikova, M.V., The role of microRNAs in the mammary gland development, health, and function of cattle, goats, and sheep, Non-Coding RNA, 2021, vol. 7, no. 4, p. 78. https://doi.org/10.3390/ncrna7040078

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Yang, B., Jiao, B., Ge, W., et al., Transcriptome sequencing to detect the potential role of long non-coding RNAs in bovine mammary gland during the dry and lactation period, BMC Genomics, 2018, vol. 19, no. 605, pp. 1—14. https://doi.org/10.1186/s12864-018-4974-5

    Article  CAS  Google Scholar 

  51. Williams, M.M., Vaught, D.B., Joly, M.M., et al., ErbB3 drives mammary epithelial survival and differentiation during pregnancy and lactation, Breast Cancer Res., 2017, vol. 19, no. 105, pp. 1—14. https://doi.org/10.1186/s13058-017-0893-7

    Article  CAS  Google Scholar 

  52. Qu, S., Yang, X., Li, X., et al., Circular RNA: a new star of noncoding RNAs, Cancer Lett., 2015, vol. 365, no. 2, pp. 141—148. https://doi.org/10.1016/j.canlet.2015.06.003

    Article  CAS  PubMed  Google Scholar 

  53. Pamudurti, N.R., Bartok, O., Jens, M., et al., Translation of CircRNAs, Mol. Cell, 2017, vol. 66, no. 1, pp. 9—21. e7. https://doi.org/10.1016/j.molcel.2017.02.021

  54. Patop, I.L., Wüst, S., and Kadener, S., Past, present, and future of circRNAs, EMBO J., 2019, vol. 38, no. 16. e100836. https://doi.org/10.15252/embj.2018100836

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. He, T., Chen, Q., Tian, K., et al., Functional role of circRNAs in the regulation of fetal development, muscle development, and lactation in livestock, BioMed Res. Int., 2021, vol. 2021. https://doi.org/10.1155/2021/5383210

  56. Liu, J., Zhang, M.L., Li, D.W., et al., Prolactin-responsive circular RNA circHIPK3 promotes proliferation of mammary epithelial cells from dairy cow, Genes, 2020, vol. 11, no. 3, p. 336. https://doi.org/10.3390/genes11030336

    Article  CAS  PubMed Central  Google Scholar 

  57. Chen, Z., Liang, Y., Lu, Q.Y., et al., Cadmium promotes apoptosis and inflammation via the circ08409/miR-133a/TGFB2 axis in bovine mammary epithelial cells and mouse mammary gland, Ecotoxicol. Environ. Saf., 2021, vol. 222, p. 112477. https://doi.org/10.1016/j.ecoenv.2021.112477

    Article  CAS  PubMed  Google Scholar 

  58. Bierne, H., Hamon, M., and Cossart, P., Epigenetics and bacterial infections, Cold Spring Harbor Perspect. Med., 2012, vol. 2, no. 12, p. a010272. https://doi.org/10.1101/cshperspect.a010272

    Article  CAS  Google Scholar 

  59. Ganguli, S. and Chakraborty, R., Bacterial epigenetics opens door to novel frontier in infection biology, Nucleus, 2021, vol. 64, no. 3, pp. 383—399. https://doi.org/10.1007/s13237-021-00375-y

    Article  CAS  Google Scholar 

  60. Grabiec, A.M. and Potempa, J., Epigenetic regulation in bacterial infections: targeting histone deacetylases, Crit. Rev. Microbiol., 2018, vol. 44, no. 3, pp. 336—350. https://doi.org/10.1080/1040841X.2017.1373063

    Article  CAS  PubMed  Google Scholar 

  61. Ząbek, T., Semik-Gurgul, E., Ropka-Molik, K., et al., Locus-specific interrelations between gene expression and DNA methylation patterns in bovine mammary gland infected by coagulase-positive and coagulase-negative staphylococci, J. Dairy Sci., 2020, vol. 103, no. 11, pp. 10689—10695. https://doi.org/10.3168/jds.2020-18404

    Article  CAS  PubMed  Google Scholar 

  62. Han, S., Li, X., Liu, J., et al., Bta-miR-223 targeting CBLB contributes to resistance to Staphylococcus aureus mastitis through the PI3K/AKT/NF-κB pathway, Front. Vet. Sci., 2020, p. 529. https://doi.org/10.3389/fvets.2020.00529

  63. Vanselow, J., Yang, W., Herrmann, J., et al., DNA-remethylation around a STAT5-binding enhancer in the αS1-casein promoter is associated with abrupt shutdown of αS1-casein synthesis during acute mastitis, J. Mol. Endocrinol., 2006, vol. 37, no. 3, pp. 463—477. https://doi.org/10.1677/jme.1.02131

    Article  CAS  PubMed  Google Scholar 

  64. Jin, W., Ibeagha-Awemu, E.M., Liang, G., et al., Transcriptome microRNA profiling of bovine mammary epithelial cells challenged with Escherichia coli or Staphylococcus aureus bacteria reveals pathogen directed microRNA expression profiles, BMC Genomics, 2014, vol. 15, no. 181, pp. 1—16. https://doi.org/10.1186/1471-2164-15-181

    Article  CAS  Google Scholar 

  65. Pispa, J. and Thesleff, I., Mechanisms of ectodermal organogenesis, Dev. Biol., 2003, vol. 262, no. 2, pp. 195—205. https://doi.org/10.1016/S0012-1606(03)00325-7

    Article  CAS  PubMed  Google Scholar 

  66. Ha, W.T., Jeong, H.Y., Lee, S.Y., and Song, H., Effects of the insulin-like growth factor pathway on the regulation of mammary gland development, Dev. Reprod., 2016, vol. 20, no. 3, pp. 179—185. https://doi.org/10.12717/DR.2016.20.3.179

    Article  PubMed  PubMed Central  Google Scholar 

  67. Rowson, A.R., Daniels, K.M., Ellis, S.E., and Ho-vey, R.C., Growth and development of the mammary glands of livestock: a veritable barnyard of opportunities, Semin. Cell Dev. Biol. Acad. Press, 2012, vol. 23, no. 5, pp. 557—566. https://doi.org/10.1016/j.semcdb.2012.03.018

    Article  Google Scholar 

  68. Capuco, A.V. and Akers, R.M., Management and environmental influences on mammary gland development and milk production, Managing the Prenatal Environment to Enhance Livestock Productivity, Dordrecht: Springer-Verlag, 2009, pp. 259—292. https://doi.org/10.1007/978-90-481-3135-8_9.

  69. Sejrsen, K., Relationships between nutrition, puberty and mammary development in cattle, Proc. Nutr. Soc., 1994, vol. 53, no. 1, pp. 103—111. https://doi.org/10.1079/PNS19940014

    Article  CAS  PubMed  Google Scholar 

  70. Veltmaat, J.M., Veelen, W.V., Thiery, J.P., and Bellusci, S., Identification of the mammary line in mouse by Wnt10b expression, Dev. Dyn., 2004, vol. 229, no. 2, pp. 349—356. https://doi.org/10.1002/dvdy.10441

    Article  CAS  PubMed  Google Scholar 

  71. Boras-Granic, K. and Wysolmerski, J.J., Wnt signaling in breast organogenesis, Organogenesis, 2008, vol. 4, no. 2, pp. 116—122. https://doi.org/10.4161/org.4.2.5858

    Article  PubMed  PubMed Central  Google Scholar 

  72. Carroll, L.S. and Capecchi, M.R., Hoxc8 initiates an ectopic mammary program by regulating Fgf10 and Tbx3 expression and Wnt/β-catenin signaling, Development, 2015, vol. 142, no. 23, pp. 4056—4067. https://doi.org/10.1242/dev.128298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Eblaghie, M.C., Song, S.J., Kim, J.Y., et al., Interactions between FGF and Wnt signals and Tbx3 gene expression in mammary gland initiation in mouse embryos, J. Anat., 2004, vol. 205, no. 1, pp. 1—13. https://doi.org/10.1111/j.0021-8782.2004.00309.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Slepicka, P.F., Somasundara, A.V.H., and Dos Santos, C.O., The molecular basis of mammary gland development and epithelial differentiation, Semin. Cell Dev. Biol. Acad. Press, 2021, vol. 114, pp. 93—112. https://doi.org/10.1016/j.semcdb.2020.09.014

    Article  Google Scholar 

  75. Cho, K.W., Kim, J.Y., Song, S.J., et al., Molecular interactions between Tbx3 and Bmp4 and a model for dorsoventral positioning of mammary gland development, Proc. Natl. Acad. Sci. U.S.A., 2006, vol. 103, no. 45, pp. 16788—16793. https://doi.org/10.1073/pnas.0604645103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Cho, K.W., Kwon, H.J., Shin, J.O., et al., Retinoic acid signaling and the initiation of mammary gland development, Dev. Biol., 2012, vol. 365, no. 1, pp. 259—266. https://doi.org/10.1016/j.ydbio.2012.02.020

    Article  CAS  PubMed  Google Scholar 

  77. Kogata, N., Oliemuller, E., Wansbury, O., and Howard, B.A., Neuregulin-3 regulates epithelial progenitor cell positioning and specifies mammary phenotype, Stem Cells Dev., 2014, vol. 23, no. 22, pp. 2758—2770. https://doi.org/10.1089/scd.2014.0082

    Article  CAS  PubMed  Google Scholar 

  78. Lee, M.Y., Sun, L., and Veltmaat, J.M., Hedgehog and gli signaling in embryonic mammary gland development, J. Mammary Gland Biol. Neoplasia, 2013, vol. 18, no. 2, pp. 133—138. https://doi.org/10.1007/s10911-013-9291-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Kazemi, H., Mining the genome of livestock species to identify markers associated with economically relevant morphological traits and breed-specific features, Diss. Thesis, 2021. https://doi.org/10.48676/unibo/amsdottorato/9688

  80. Asselin-Labat, M.L., Sutherland, K.D., Barker, H., et al., Gata-3 is an essential regulator of mammary-gland morphogenesis and luminal-cell differentiation, Nat. Cell Biol., 2007, vol. 9, no. 2, pp. 201—209. https://doi.org/10.1038/ncb1530

    Article  CAS  PubMed  Google Scholar 

  81. Hiremath, M., Dann, P., Fischer, J., et al., Parathyroid hormone-related protein activates Wnt signaling to specify the embryonic mammary mesenchyme, Development, 2012, vol. 139, no. 22, pp. 4239—4249. https://doi.org/10.1242/dev.080671

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Tickle, C. and Jung, H.S., Embryonic Mammary Gland Development, Chichester: Wiley, 2016. https://doi.org/10.1002/9780470015902.a0026057.

  83. Hiremath, M. and Wysolmerski, J., Role of PTHrP in mammary gland development and breast cancer, Clin. Rev. Bone Miner. Metab., 2014, vol. 12, no. 3, pp. 178—189. https://doi.org/10.1007/s12018-014-9170-9

    Article  CAS  Google Scholar 

  84. Denicol, A.C., Dobbs, K.B., McLean, K.M., et al., Canonical WNT signaling regulates development of bovine embryos to the blastocyst stage, Sci. Rep., 2013, vol. 3, no. 1266, pp. 1—7. https://doi.org/10.1038/srep01266

    Article  CAS  Google Scholar 

  85. Boras-Granic, K., Chang, H., Grosschedl, R., and Hamel, P.A., Lef1 is required for the transition of Wnt signaling from mesenchymal to epithelial cells in the mouse embryonic mammary gland, Dev. Biol., 2006, vol. 295, no. 1, pp. 219—231. https://doi.org/10.1016/j.ydbio.2006.03.030

    Article  CAS  PubMed  Google Scholar 

  86. Lindvall, C., Zylstra, C.R., Evans, N., et al., The Wnt co-receptor Lrp6 is required for normal mouse mammary gland development, PLoS One, 2009, vol. 4, no. 6. e5813. https://doi.org/10.1371/J..pone.0005813

    Article  PubMed  PubMed Central  Google Scholar 

  87. Ahn, Y., Sims, C., Logue, J.M., et al., Lrp4 and Wise interplay controls the formation and patterning of mammary and other skin appendage placodes by modulating Wnt signaling, Development, 2013, vol. 140, no. 3, pp. 583—593. https://doi.org/10.1242/dev.085118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Yanagita, M., Oka, M., Watabe, T., et al., USAG-1: a bone morphogenetic protein antagonist abundantly expressed in the kidney, Biochem. Biophys. Res. Commun., 2004, vol. 316, no. 2, pp. 490—500. https://doi.org/10.1016/j.bbrc.2004.02.075

    Article  CAS  PubMed  Google Scholar 

  89. Itasaki, N. and Hoppler, S., Crosstalk between Wnt and bone morphogenic protein signaling: a turbulent relationship, Dev. Dyn., 2010, vol. 239, no. 1, pp. 16—33. https://doi.org/10.1002/dvdy.22009

    Article  CAS  PubMed  Google Scholar 

  90. Gurgul, A., Jasielczuk, I., Semik-Gurgul, E., et al., Diversifying selection signatures among divergently selected subpopulations of Polish Red cattle, J. Appl. Genet., 2019, vol. 60, no. 1, pp. 87—95. https://doi.org/10.1007/s13353-019-00484-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Gordon, M.D. and Nusse, R., Wnt signaling: multiple pathways, multiple receptors, and multiple transcription factors, J. Biol. Chem., 2006, vol. 281, no. 32, pp. 22429—22433. https://doi.org/10.1074/jbc.R600015200

    Article  CAS  PubMed  Google Scholar 

  92. Niehrs, C., Function and biological roles of the Dickkopf family of Wnt modulators, Oncogene, 2006, vol. 25, no. 57, pp. 7469—7481. https://doi.org/10.1038/sj.onc.1210054

    Article  CAS  PubMed  Google Scholar 

  93. Hens, J., Dann, P., Hiremath, M., et al., Analysis of gene expression in PTHrP–/– mammary buds supports a role for BMP signaling and MMP2 in the initiation of ductal morphogenesis, Dev. Dyn., 2009, vol. 238, no. 11, pp. 2713—2724. https://doi.org/10.1002/dvdy.22097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Heckman, B.M., Chakravarty, G., Vargo-Gogola, T., et al., Crosstalk between the p190-B RhoGAP and IGF signaling pathways is required for embryonic mammary bud development, Dev. Biol., 2007, vol. 309, no. 1, pp. 137—149. https://doi.org/10.1016/j.ydbio.2007.07.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Knabel, M., Kolle, S., and Sinowatz, F., Expression of growth hormone receptor in the bovine mammary gland during prenatal development, Anat. Embryol., 1998, vol. 198, no. 2, pp. 163—169. https://doi.org/10.1007/s004290050174

    Article  CAS  Google Scholar 

  96. Speroni, L., Voutilainen, M., Mikkola, M.L., et al., New insights into fetal mammary gland morphogenesis: differential effects of natural and environmental estrogens, Sci. Rep., 2017, vol. 7, no. 40806, pp. 1—7. https://doi.org/10.1038/srep40806

    Article  CAS  Google Scholar 

  97. Brisken, C. and O’Malley, B., Hormone action in the mammary gland, Cold Spring Harbor Perspect. Biol., 2010, vol. 2, no. 12, p. a003178. https://doi.org/10.1101/cshperspect.a003178

    Article  CAS  Google Scholar 

  98. Gu, B., Sun, P., Yuan, Y., et al., Pygo2 expands mammary progenitor cells by facilitating histone H3 K4 methylation, J. Cell Biol., 2009, vol. 185, no. 5, pp. 811—826. https://doi.org/10.1083/jcb.200810133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Lee, M.J., Yoon, K.S., Cho, K.W., et al., Expression of miR-206 during the initiation of mammary gland development, Cell Tissue Res., 2013, vol. 353, no. 3, pp. 425—433. https://doi.org/10.1007/s00441-013-1653-3

    Article  CAS  PubMed  Google Scholar 

  100. Lee, J.M., Cho, K.W., Kim, E.J., et al., A contrasting function for miR-137 in embryonic mammogenesis and adult breast carcinogenesis, Oncotarget, 2015, vol. 6, no. 26, pp. 22048—22059. https://doi.org/10.18632/oncotarget.4218

    Article  PubMed  PubMed Central  Google Scholar 

  101. Sejrsen, K., Huber, J.T., and Tucker, H.A., Influence of amount fed on hormone concentrations and their relationship to mammary growth in heifers, J. Dairy Sci., 1983, vol. 66, no. 4, pp. 845—855. https://doi.org/10.3168/jds.S0022-0302(83)81866-9

    Article  CAS  PubMed  Google Scholar 

  102. Geiger, A.J., The pre-pubertal bovine mammary gland: unlocking the potential of the future herd, Animal, 2019, vol. 13, no. S1, pp. s4—s10. https://doi.org/10.1017/S1751731119001204

    Article  CAS  PubMed  Google Scholar 

  103. Choudhary, R.K., Identification and Characterization of Presumptive Bovine Mammary Stem Cells, College Park: Univ. Maryland, 2011.

    Google Scholar 

  104. Capuco, A.V. and Ellis, S., Bovine mammary progenitor cells: current concepts and future directions, J. Mammary Gland Biol. Neoplasia, 2005, vol. 10, no. 1, pp. 5—15. https://doi.org/10.1007/s10911-005-2536-3

    Article  CAS  PubMed  Google Scholar 

  105. Yart, L., Lollivier, V., Marnet, P.G., and Dessauge, F., Role of ovarian secretions in mammary gland development and function in ruminants, Animal, 2014, vol. 8, no. 1, pp. 72—85. https://doi.org/10.1017/S1751731113001638

    Article  CAS  PubMed  Google Scholar 

  106. McNally, S. and Martin, F., Molecular regulators of pubertal mammary gland development, Ann. Med., 2011, vol. 43, no. 3, pp. 212—234. https://doi.org/10.3109/07853890.2011.554425

    Article  PubMed  Google Scholar 

  107. Daniels, K.M., Capuco, A.V., McGilliard, M.L., et al., Effects of milk replacer formulation on measures of mammary growth and composition in Holstein heifers, J. Dairy Sci., 2009, vol. 92, no. 12, pp. 5937—5950. https://doi.org/10.3168/jds.2008-1959

    Article  CAS  PubMed  Google Scholar 

  108. Hovey, R.C., Trott, J.F., and Vonderhaar, B.K., Establishing a framework for the functional mammary gland: from endocrinology to morphology, J. Mammary Gland Biol. Neoplasia, 2002, vol. 7, no. 1, pp. 17—38. https://doi.org/10.1023/A:1015766322258

    Article  PubMed  Google Scholar 

  109. Sinha, Y.N. and Tucker, H.A., Mammary development and pituitary prolactin level of heifers from birth through puberty and during the estrous cycle, J. Dairy Sci., 1969, vol. 52, no. 4, pp. 507—512. https://doi.org/10.3168/jds.S0022-0302(69)86595-1

    Article  CAS  PubMed  Google Scholar 

  110. Kostomakhin, N. and Samoilenko, T., Dependence of milk productivity of cows on their age and live weight at the first insemination, Korma Korml., 2008, no. 11, pp. 15—18.

  111. Akers, R.M., Lactation and the mammary gland, Protoplasma, 2016, vol. 159, pp. 96—111. https://doi.org/10.1002/9781119264880

    Article  Google Scholar 

  112. Howlin, J., McBryan, J., and Martin, F., Pubertal mammary gland development: insights from mouse models, J. Mammary Gland Biol. Neoplasia, 2006, vol. 11, no. 3, pp. 283—297. https://doi.org/10.1007/s10911-006-9024-2

    Article  PubMed  Google Scholar 

  113. Dahl, G.E., Physiology of lactation in dairy cattle-challenges to sustainable production, Anim. Agric. Acad. Press, 2020, pp. 121—129. https://doi.org/10.1016/B978-0-12-817052-6.00007-0

  114. Kuz’mich, R.G., Rubanets, L.N., Garbuzov, A.A., and Yushkovskii, E.A., Bolezni yaichnikov i yaitsevodov u korov (Ovarian and Oviduct Pathologies in Cows), Vitebsk, 2017.

    Google Scholar 

  115. Mallepell, S., Krust, A., Chambon, P., and Brisken, C., Paracrine signaling through the epithelial estrogen receptor α is required for proliferation and morphogenesis in the mammary gland, Proc. Natl. Acad. Sci. U.S.A., 2006, vol. 103, no. 7, pp. 2196—2201. https://doi.org/10.1073/pnas.0510974103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Fata, J.E., Chaudhary, V., and Khokha, R., Cellular turnover in the mammary gland Is correlated with systemic levels of progesterone and Not 17β-estradiol during the estrous cycle, Biol. Reprod., 2001, vol. 65, no. 3, pp. 680—688. https://doi.org/10.1095/biolreprod65.3.680

    Article  CAS  PubMed  Google Scholar 

  117. Capuco, A.V., Ellis, S., Wood, D.L., et al., Postnatal mammary ductal growth: three-dimensional imaging of cell proliferation, effects of estrogen treatment, and expression of steroid receptors in prepubertal calves, Tissue Cell, 2002, vol. 34, no. 3, pp. 143—154. https://doi.org/10.1016/S0040-8166(02)00024-1

    Article  CAS  PubMed  Google Scholar 

  118. Meyer, M.J., Capuco, A.V., Boisclair, Y.R., and Van Amburgh, M.E., Estrogen-dependent responses of the mammary fat pad in prepubertal dairy heifers, J. Endocrinol., 2006, vol. 190, no. 3, pp. 819—827. https://doi.org/10.1677/joe.1.06883

    Article  CAS  PubMed  Google Scholar 

  119. Connor, E.E., Wood, D.L., Sonstegard, T.S., et al., Chromosomal mapping and quantitative analysis of estrogen-related receptor alpha-1, estrogen receptors alpha and beta and progesterone receptor in the bovine mammary gland, J. Endocrinol., 2005, vol. 185, no. 3, pp. 593—603. https://doi.org/10.1677/joe.1.06139

    Article  CAS  PubMed  Google Scholar 

  120. Wallace, C., Observations on mammary development in calves and lambs, J. Agric. Sci., 1953, vol. 43, no. 4, pp. 413—421. https://doi.org/10.1017/S0021859600057890

    Article  Google Scholar 

  121. Purup, S., Sejrsen, K., Foldager, J., and Akers, R.M., Effect of exogenous bovine growth hormone and ovariectomy on prepubertal mammary growth, serum hormones and acute in vitro proliferative response of mammary explants from Holstein heifers, J. Endocrinol., 1993, vol. 139, no. 1, pp. 19—26. https://doi.org/10.1677/joe.0.1390019

    Article  CAS  PubMed  Google Scholar 

  122. Berry, S.D.K., Jobst, P.M., Ellis, S.E., et al., Mammary epithelial proliferation and estrogen receptor α expression in prepubertal heifers: effects of ovariectomy and growth hormone, J. Dairy Sci., 2003, vol. 86, no. 6, pp. 2098—2105. https://doi.org/10.3168/jds.S0022-0302(03)73799-0

    Article  CAS  PubMed  Google Scholar 

  123. Ballagh, S.D.K., Jobst, P.M., Ellis, S.E., et al., Hot topic: prepubertal ovariectomy alters the development of myoepithelial cells in the bovine mammary gland, J. Dairy Sci., 2008, vol. 91, no. 8, pp. 2992—2995. https://doi.org/10.3168/jds.2008-1191

    Article  CAS  PubMed  Google Scholar 

  124. Sud, S.C., Tucker, H.A., and Meites, J., Estrogen-progesterone requirements for udder development in ovariectomized heifers, J. Dairy Sci., 1968, vol. 51, no. 2, pp. 210—214. https://doi.org/10.3168/jds.S0022-0302(68)86954-1

    Article  CAS  PubMed  Google Scholar 

  125. Woodward, T.L., Beal, W.E., and Akers, R.M., Cell interactions in initiation of mammary epithelial proliferation by oestradiol and progesterone in prepubertal heifers, J. Endocrinol., 1993, vol. 136, no. 1, pp. 149—157. https://doi.org/10.1677/joe.0.1360149

    Article  CAS  PubMed  Google Scholar 

  126. Li, R.W., Meyer, M.J., Van Tassell, C.P., et al., Identification of estrogen-responsive genes in the parenchyma and fat pad of the bovine mammary gland by microarray analysis, Physiol. Genomics, 2006, vol. 27, no. 1, pp. 42—53. https://doi.org/10.1152/physiolgenomics.00032.2006

    Article  CAS  PubMed  Google Scholar 

  127. Purup, S., Sejrsen, K., and Akers, R.M., Effect of bovine GH and ovariectomy on mammary tissue sensitivity to IGF-I in prepubertal heifers, J. Endocrinol., 1995, vol. 144, no. 1, pp. 153—158. https://doi.org/10.1677/joe.0.1440153

    Article  CAS  PubMed  Google Scholar 

  128. Silva, L.F.P., Liesman, J.S., Etchebarne, B.E., et al., Intramammary infusion of IGF-I increases bromodeoxyuridine labeling in mammary epithelial cells of prepubertal heifers, J. Dairy Sci., 2005, vol. 88, no. 8, pp. 2771—2773. https://doi.org/10.3168/jds.S0022-0302(05)72956-8

    Article  CAS  PubMed  Google Scholar 

  129. Greenwood, P.L., Bell, A.W., Vercoe, P.E., and Viljoen, G.J., Managing the Prenatal Environment to Enhance Livestock Productivity, Dordrecht: Springer-Verlag, 2010. https://doi.org/10.1007/978-90-481-3135-8

    Book  Google Scholar 

  130. Purup, S., Vestergaard, M., and Sejrsen, K., Involvement of growth factors in the regulation of pubertal mammary growth in cattle, Biol. Mammary Gland, 2002, vol. 480, pp. 27—43. https://doi.org/10.1007/0-306-46832-8_4

    Article  Google Scholar 

  131. Roith, D.L., The insulin-like growth factor system, Exp. Diabetes Res., 2003, vol. 4, no. 4, pp. 205—212. https://doi.org/10.1155/EDR.2003.205

    Article  Google Scholar 

  132. Berry, S.D., McFadden, T.B., Pearson, R.E., and Akers, R.M., A local increase in the mammary IGF-1: IGFBP-3 ratio mediates the mammogenic effects of estrogen and growth hormone, Domest. Anim. Endocrinol., 2001, vol. 21, no. 1, pp. 39—53. https://doi.org/10.1016/S0739-7240(01)00101-1

    Article  CAS  PubMed  Google Scholar 

  133. Plath, A., Einspanier, R., Peters, F., et al., Expression of transforming growth factors alpha and beta-1 messenger RNA in the bovine mammary gland during different stages of development and lactation, J. Endocrinol., 1997, vol. 155, pp. 501—511. https://doi.org/10.1677/joe.0.1550501

    Article  CAS  PubMed  Google Scholar 

  134. Sivaprasad, U., Fleming, J., Verma, P.S., et al., Stimulation of insulin-like growth factor (IGF) binding protein-3 synthesis by IGF-I and transforming growth factor-α is mediated by both phosphatidylinositol-3 kinase and mitogen-activated protein kinase pathways in mammary epithelial cells, Endocrinology, 2004, vol. 145, no. 9, pp. 4213—4221. https://doi.org/10.1210/en.2003-1377

    Article  CAS  PubMed  Google Scholar 

  135. Booth, B.W., Boulanger, C.A., Anderson, L.H., et al., Amphiregulin mediates self-renewal in an immortal mammary epithelial cell line with stem cell characteristics, Exp. Cell Res., 2010, vol. 316, no. 3, pp. 422—432. https://doi.org/10.1016/j.yexcr.2009.11.006

    Article  CAS  PubMed  Google Scholar 

  136. Kouros-Mehr, H., Slorach, E.M., Sternlicht, M.D., and Werb, Z., GATA-3 maintains the differentiation of the luminal cell fate in the mammary gland, Cell, 2006, vol. 127, no. 5, pp. 1041—1055. https://doi.org/10.1016/j.cell.2006.09.048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Pietersen, A.M., Evers, B., Prasad, A.A., et al., Bmi1 regulates stem cells and proliferation and differentiation of committed cells in mammary epithelium, Curr. Biol., 2008, vol. 18, no. 14, pp. 1094—1099. https://doi.org/10.1016/j.cub.2008.06.070

    Article  CAS  PubMed  Google Scholar 

  138. Huang, D.W., Sherman, B.T., Tan, Q., et al., DAVID bioinformatics resources: expanded annotation database and novel algorithms to better extract biology from large gene lists, Nucleic Acids Res., 2007, vol. 35, suppl. 2, pp. W169—W175. https://doi.org/10.1093/nar/gkm415

    Article  PubMed  PubMed Central  Google Scholar 

  139. Li, W., Li, C., Lu, J., and Zhao, W., MiR-145 is involved in the proliferation of bovine mammary epithelial cells and regulates bovine insulin receptor substrate 1, Ital. J. Anim. Sci., 2020, vol. 19, no. 1, pp. 536—543. https://doi.org/10.1080/1828051X.2020.1732234

    Article  CAS  Google Scholar 

  140. Ucar, A., Vafaizadeh, V., Jarry, H., et al., miR-212 and miR-132 are required for epithelial stromal interactions necessary for mouse mammary gland development, Nat. Genet., 2010, vol. 42, no. 12, pp. 1101—1108. https://doi.org/10.1038/ng.709

    Article  CAS  PubMed  Google Scholar 

  141. Wicik, Z., Gajewska, M., Majewska, A., et al., Characterization of microRNA profile in mammary tissue of dairy and beef breed heifers, J. Anim. Breed. Genet., 2016, vol. 133, no. 1, pp. 31—42. https://doi.org/10.1111/jbg.12172

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

The research has been supported by State Order. Registration number of the topic “Assessment of Genetic Potential of National Cattle Breeds” is 122020800034-4.

The research has been supported by the complex science and technology program of the Ministry of Education and Science of the Russian Federation.

Author information

Authors and Affiliations

  1. Vavilov Institute of General Genetics, Russian Academy of Sciences, 119991, Moscow, Russia

    E. V. Solodneva, S. B. Kuznetsov & Yu. A. Stolpovsky

  2. Student at the School of Engineering and Applied Sciences, University of Pennsylvania, PA 19104, Philadelphia, USA

    A. E. Velieva

Authors
  1. E. V. Solodneva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. B. Kuznetsov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. E. Velieva
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yu. A. Stolpovsky
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. V. Solodneva.

Ethics declarations

The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

Additional information

Translated by E. Makeeva

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Solodneva, E.V., Kuznetsov, S.B., Velieva, A.E. et al. Molecular-Genetic Bases of Mammary Gland Development Using the Example of Cattle and Other Animal Species: I. Embryonic and Pubertal Developmental Stage. Russ J Genet 58, 899–914 (2022). https://doi.org/10.1134/S1022795422080087

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1022795422080087

Keywords:

Search

Navigation