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Suppression of ovarian secretions before puberty strongly affects mammogenesis in the goat

Published online by Cambridge University Press:  20 February 2012

Lucile Yart ,
Laurence Finot ,
Pierre-Guy Marnet  and
Frédéric Dessauge
Lucile Yart
Affiliation:
INRA UMR 1080 Dairy Production, F-35000 Rennes, France AGROCAMPUS UMR 1080 Dairy Production, F-35000 Rennes, France
Laurence Finot
Affiliation:
INRA UMR 1080 Dairy Production, F-35000 Rennes, France AGROCAMPUS UMR 1080 Dairy Production, F-35000 Rennes, France
Pierre-Guy Marnet
Affiliation:
INRA UMR 1080 Dairy Production, F-35000 Rennes, France AGROCAMPUS UMR 1080 Dairy Production, F-35000 Rennes, France
Frédéric Dessauge*
Affiliation:
INRA UMR 1080 Dairy Production, F-35000 Rennes, France AGROCAMPUS UMR 1080 Dairy Production, F-35000 Rennes, France
*
*For correspondence; e-mail: [email protected]
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Abstract

The objective of this study was to provide insight into the biological mechanisms underlying mammary development and the role of the ovaries in prepubertal caprine mammogenesis using a serial ovariectomy approach. Young Alpine goats were ovariectomized (Ovx) or sham-operated (Int) at three periods before puberty (G1=1 month, G2=2 month and G3=3 months of age) and one after puberty (G7=7 months of age). The goats were slaughtered at 9 months of age and mammary glands were removed. Ovariectomy performed at 1, 2 and 3 months of age caused a 50% reduction in DNA concentration, in mammary tissue taken from the parenchyma-stroma border region. Morphological analysis of mammary tissue sections indicated that the parenchymal structures of Ovx goats were negatively affected by ovariectomy. Goats ovariectomized before 2 months of age (Ovx-1 and Ovx-2) showed a significant decrease in the percent of cells proliferating in mammary glands of 9-month old goats (proliferating cell nuclear antigen expression and antigen Ki67-positive cell number). Also, goats ovariectomized at 1 and 2 months of age had reduced matrix metalloprotease 2 activity at 9 months of age. E-cadherin was strongly decreased in goats ovariectomized before 2 months of age (80 and 85% in Ovx-1 and Ovx-2 goats, respectively). Quantitative PCR analysis of transcripts encoding for oestrogen (ERα) and progesterone receptors (PR) and immunodetection of ERα showed that ovariectomy at 1 and 2 months of age strongly inhibited the transcription of ERα and PR in the mammary gland. We conclude that ovariectomy before 3 months of age markedly impaired parenchymal development. These findings suggest that prepubertal mammogenesis in goats depends on the ovaries to initiate mammary epithelial cell proliferation and mammary gland remodelling.

Keywords

Dairy goatpubertyovariectomymammary parenchymal development
Type
Research Article
Information
Journal of Dairy Research , Volume 79 , Issue 2 , May 2012 , pp. 157 - 167
Copyright
Copyright © Proprietors of Journal of Dairy Research 2012

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References

Akers, RM 1985 Lactogenic– hormones: binding sites, mammary growth, secretory cell differentiation, and milk biosynthesis in ruminants. Journal of Dairy Science 68 501–519CrossRefGoogle ScholarPubMed
Akers, R, Ellis, S & Berry, S 2005 Ovarian and IGF-I axis control of mammary development in prepubertal heifers. Domestic Animal Endocrinology 29 259–267CrossRefGoogle ScholarPubMed
Berry, SD, Jobst, PM, Ellis, SE, Howard, RD, Capuco, AV, & Akers, RM 2003 Mammary epithelial proliferation and estrogen receptor alpha expression in prepubertal heifers: effects of ovariectomy and growth hormone. Journal of Dairy Science 86 2098–2105CrossRefGoogle ScholarPubMed
Berry, SD, McFadden, TB, Pearson, RE & Akers, RM 2001 A local increase in the mammary IGF-1: IGFBP-3 ratio mediates the mammogenic effects of estrogen and growth hormone. Domestic Animal Endocrinology 21 39–53CrossRefGoogle ScholarPubMed
Capuco, AV, Ellis, S, Wood, DL, Akers, RM & Garrett, W 2002 Postnatal mammary ductal growth: three-dimensional imaging of cell proliferation, effects of estrogen treatment, and expression of steroid receptors in prepubertal calves. Tissue Cell 34 143–154CrossRefGoogle ScholarPubMed
Connor, EE, Meyer, MJ, Li, RW, Van Amburgh, ME, Boisclair, YR & Capuco, AV 2007 Regulation of gene expression in the bovine mammary gland by ovarian steroids. Journal of Dairy Science 90 Suppl. 1E55–E65CrossRefGoogle ScholarPubMed
Dessauge, F, Finot, L, Wiart, S, Aubry, JM & Ellis, SE 2009 Effects of ovariectomy in prepubertal goats. Journal of Physiology and Pharmacology 60 Suppl. 3127–133Google ScholarPubMed
Ellis, S, McFadden, TB & Akers, RM 1998 Prepuberal ovine mammary development is unaffected by ovariectomy. Domestical Animal Endocrinology 15 217–225CrossRefGoogle ScholarPubMed
Erb, RE 1977 Hormonal control of mammogenesis and onset of lactation in cows – a review. Journal of Dairy Science 60 155–169CrossRefGoogle ScholarPubMed
Kastner, P, Krust, A, Turcotte, B, Stropp, U, Tora, L, Gronemeyer, H & Chambon, P 1990 Two distinct estrogen-regulated promoters generate transcripts encoding the two functionally different human progesterone receptor forms A and B. EMBO Journal 9 1603–1614CrossRefGoogle ScholarPubMed
Korach, KS 1994 Insights from the study of animals lacking functional estrogen receptor. Science 266 1524–1527CrossRefGoogle Scholar
Meyer, MJ, Capuco, AV, Boisclair, YR & Van Amburgh, ME 2006 Estrogen-dependent responses of the mammary fat pad in prepubertal dairy heifers. Journal of Endocrinology 190 819–827CrossRefGoogle ScholarPubMed
Monteagudo, C, Merino, M, San-Juan, J, Liotta, L & Stetler-Stevenson, W 1990 Immunohistochemica distribution of type IV collagenase in normal, begnin, and malignant breast tissue. American Journal of Pathology 136 585–592(Abstr.)Google Scholar
Petz, LN, Ziegler, YS, Schultz, JR, Kim, H, Kemper, JK & Nardulli, AM 2004 Differential regulation of the human progesterone receptor gene through an estrogen response element half site and Sp1 sites. Journal of Steroid Biochemistry and Molecular Biology 88 113–122CrossRefGoogle ScholarPubMed
Pfaffl, MW 2001 A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29 e45CrossRefGoogle ScholarPubMed
Purup, S, Sejrsen, K & Akers, RM 1995 Effect of bovine GH and ovariectomy on mammary tissue sensitivity to IGF-I in prepubertal heifers. Journal of Endocrinology 144 153–158CrossRefGoogle ScholarPubMed
Purup, S, Sejrsen, K, Foldager, J & Akers, RM 1993 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. Journal of Endocrinology 139 19–26CrossRefGoogle ScholarPubMed
Rabot, A, Sinowatz, F, Berisha, B, Meyer, HH & Schams, D 2007 Expression and localization of extracellular matrix-degrading proteinases and their inhibitors in the bovine mammary gland during development, function, and involution. Journal of Dairy Science 90 740–748CrossRefGoogle ScholarPubMed
Robinson, TL, Sutherland, IA & Sutherland, J 2007 Validation of candidate bovine reference genes for use with real-time PCR. Veterinary Immunology and Immunopathology 115 160–165CrossRefGoogle ScholarPubMed
Romagnolo, D, Akers, RM, Wong, EA, Boyle, PL, McFadden, TB, Byatt, JC & Turner, JD 1993 Lactogenic hormones and extracellular matrix regulate expression of IGF-1 linked to MMTV-LTR in mammary epithelial cells. Molecular and Cellular Endocrinology 96 147–157CrossRefGoogle ScholarPubMed
Rudolph-Owen, L & Matrisian, L 1998 Matrix metalloproteinase in remodeling of the normal and neoplastic mammary gland. Journal of Mammary Gland Biology and Neoplasia 3 177–189CrossRefGoogle ScholarPubMed
Samulin, J, Berget, I, Lien, S & Sundvold, H 2008 Differential gene expression of fatty acid binding proteins during porcine adipogenesis. Comparative Biochemistry and Physiology 151 147–152CrossRefGoogle ScholarPubMed
Sinha, YN & Tucker, HA 1969 Mammary development and pituitary prolactin level of heifers from birth through puberty and during the estrous cycle. Journal of Dairy Science 52 507–512CrossRefGoogle ScholarPubMed
Sympson, C, Talhouk, R, Alexander, C, Chin, J, Clift, S, Bissell, M & Werb, Z 1994 Targeted expression of Stromelysin-1 in mammary gland provides evidence for a role of proteinases in branching morphogenesis and the requirement for an intact basement membrane for tissue-specific gene expression. Journal of Cell Biology 125 681–693CrossRefGoogle ScholarPubMed
Vandesompele, J, De Preter, K, Pattyn, F, Poppe, B, Van Roy, N, De Paepe, A & Speleman, F 2002 Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3 RESEARCH0034CrossRefGoogle ScholarPubMed
Wallace, C 1953 Observations on mammary development in calves and lambs. Journal of Agricultural Science 43 413–421(Abstr.)CrossRefGoogle Scholar
Wiseman, BS, Sternlicht, MD, Lund, LR, Alexander, CM, Mott, J, Bissell, MJ, Soloway, P, Itohara, S & Werb, Z 2003 Site-specific inductive and inhibitory activities of MMP-2 and MMP-3 orchestrate mammary gland branching morphogenesis. Journal of Cellular Biology 162 1123–1133CrossRefGoogle ScholarPubMed
Witty, J, Wright, J & Matrisian, L 1995 Matrix metalloproteinases are expressed during ductal and alveolar mammary morphogenesis, and misregulation of stromelysin-1 in transgenic mice induces unscheduled alveolas development. Molecular Biology of the Cell 6 1287–1303(Abstr.)CrossRefGoogle Scholar
Woodward, TL, Beal, WE & Akers, RM 1993 Cell interactions in initiation of mammary epithelial proliferation by oestradiol and progesterone in prepubertal heifers. Journal of Endocrinology 136 149–157CrossRefGoogle ScholarPubMed