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Role of ovarian secretions in mammary gland development and function in ruminants*

  • L. Yart (a1) (a2), V. Lollivier (a1) (a2), P. G. Marnet (a1) (a2) and F. Dessauge (a1) (a2)

Abstract

The mammary gland is a dynamic organ that undergoes cyclic developmental and regressive changes during the lifetime of a female mammal. Mammogenesis begins during embryonic life with the development of the first mammary gland rudiments and ductal system. After birth, during the pre-pubertal period, the ductal growth of the mammary parenchyma occurs through the fat pad. In most of the ruminant species allometric mammary parenchyma development begins with the onset of cyclic ovarian secretions activity. The two main hormones secreted during an ovarian cycle are estradiol and progesterone. These steroid hormones are derived from cholesterol and are synthesized by theca and granulosa cells in ovaries. During puberty, the mammary parenchyma develops in a compact, highly arborescent parenchymal mass surrounded by a dense connective matrix. Ductal elongation and lobulo-alveolar development are accomplished during growth and pregnancy to prepare for future milk production. At the end of lactation, the mammary gland undergoes involution, which corresponds to a regression of the secretory tissue, a reduction in the alveolar size and a loss of mammary epithelial cells (MECs). Ovarian steroids (estradiol and progesterone) appear to be key regulators of the different stages of mammogenesis and mammary function. Through this review, the role and the importance of ovarian steroids on mammary gland and on MECs is described.

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This review comes from the 63rd European Federation of Animal Science EAAP Annual Meeting, Bratislava, Slovak Republic, 27–31 August 2012.

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Accorsi, PA, Pacioni, B, Pezzi, C, Forni, M, Flint, DJ and Seren, E 2002. Role of prolactin, growth hormone and insulin-like growth factor 1 in mammary gland involution in the dairy cow. Journal of Dairy Science 85, 507513.
Akers, RM, Ellis, SE and Berry, SDK 2005. Ovarian and IGF-I axis control of mammary development in prepubertal heifers. Domestic Animal Endocrinology 29, 259267.
Akers, RM, Beal, WE, McFadden, TB and Capuco, AV 1990. Morphometric analysis of involuting bovine mammary tissue after 21 or 42 days on non-suckling. Journal of Animal Science 68, 36043613.
Akers, RM, Bauman, DE, Capuco, AV, Goodman, GT and Tucker, HA 1981a. Prolactin regulation of milk secretion and biochemical differentiation of mammary epithelial cells in periparturient cows. Endocrinology 109, 2330.
Akers, RM, Bauman, DE, Goodman, GT, Capuco, AV and Tucker, HA 1981b. Prolactin regulation of cytological differentiation of mammary epithelial cells in periparturient cows. Endocrinology 109, 3140.
Ambili, M, Jayasree, K and Sudhakaran, PR 1998. 60 k gelatinase involved in mammary gland involution is regulated by beta-oestradiol. Biochemica et Biophysica 1403, 219231.
Anderson, E, Clarke, RB and Howell, A 1998. Estrogen responsiveness and control of normal human breast proliferation. Journal of Mammary Gland Biology and Neoplasia 3, 2335.
Annen, EL, Fitzgerald, AC, Gentry, PC, McGuire, MA, Capuco, AV, Baumgard, LH and Collier, RJ 2007. Effect of continuous milking and bovine somatotropin supplementation on mammary epithelial cell turnover. Journal of Dairy Science 90, 165183.
Athie, F, Bachman, KC, Head, HH, Hayen, MJ and Wilcox, CJ 1996. Estrogen administrated at final milk removal accelerates involution of bovine mammary gland. Journal of Dairy Science 79, 220226.
Atwood, CS, Hovey, RC, Glover, JP, Chepko, G, Ginsburg, E, Robison, WG and Vonderhaar, BK 2000. Progesterone induces side-branching of the ductal epithelium in the mammary glands of peripubertal mice. Journal of Endocrinology 167, 3952.
Auldist, MJ, Turner, SA, McMahon, CD and Prosser, CG 2007. Effects of melatonin on the yield and composition of milk from grazing dairy cows in New Zealand. Journal of Dairy Research 74, 5257.
Aupperlee, MD and Haslam, SZ 2007. Differential hormonal regulation and function of progesterone receptor isoforms in normal adult mouse mammary gland. Endocrinology 148, 22902300.
Bachman, KC, Hayen, MJ, Morse, D and Wilcox, CJ 1988. Effect of pregnancy, milk yield and somatic cell count on bovine milk fat hydrolysis. Journal of Dairy Science 71, 925931.
Baril, G, Leboeuf, B and Saumande, J 1993. Synchronization of estrus in goats: the relationship between time of occurrence of estrus and fertility following artificial insemination. Theriogenology 40, 621628.
Bartlewski, PM, Baby, TE and Giffin, JL 2011. Reproductive cycles in sheep. Animal Reproduction Science 124, 259268.
Bazer, FW and First, NL 1983. Pregnancy and parturition. Journal of Animal Science 57 (suppl. 2), 425460.
Benoit, AM, Inskeep, EK and Dailey, RA 1992. Effect of a nonsteroidal aromatase inhibitor on invitro and invivo secretion of estradiol and on the estrous-cycle in ewes. Domestic Animal Endocrinology 9, 313327.
Bernier-Dodier, P, Delbecchi, L, Wagner, GF, Talbot, BG and Lacasse, P 2010. Effect of milking frequency on lactation persistency and mammary gland remodeling in mid-lactation cows. Journal of Dairy Science 93, 555564.
Berry, SD, McFadden, TB, Pearson, RE and 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, 3953.
Berry, SDK, Jobst, PM, Ellis, SE, Howard, RD, Capuco, AV and Akers, RM 2003a. Mammary epithelial proliferation and estrogen receptor alpha expression in prepubertal heifers: effects of ovariectomy and growth hormone. Journal of Dairy Science 86, 20982105.
Berry, SDK, Weber Nielsen, MS, Sejrsen, K, Pearson, RE, Boyle, PL and Akers, RM 2003b. Use of an immortalized bovine mammary epithelial cell line (MAC-T) to measure the mitogenic activity of extracts from heifer mammary tissue: effects of nutrition and ovariectomy. Domestic Animal Endocrinology 25, 245253.
Bertilsson, J, Berglund, B, Ratnayake, G, Svennersten Sjaunja, K and Wiktorsson, H 1997. Optimising lactation cycles for the high-yielding dairy cow. A European perspective. Livestock Production Science 50, 513.
Brisken, C and O’Malley, B 2010. Hormone action in the mammary gland. Cold Spring Harbor Perspectives in Biology 2, 12p.
Brisken, C, Heineman, A, Chavarria, T, Elenbaas, B, Tan, J, Dey, SK, McMahon, JA, McMahon, AP and Weinberg, RA 2000. Essential function of Wnt-4 in mammary gland development downstream of progesterone signaling. Genes & Development 14, 650654.
Capuco, AV, Wood, D, Baldwin, R, McLeod, K and Paape, M 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.
Capuco, AV, Ellis, S, Wood, DL, Akers, RM and Garrett, W 2002a. Postnatal mammary ductal growth: three-dimensional imaging of cell proliferation, effects of estrogen treatment, and expression of steroid receptors in prepubertal calves. Tissue and Cell 34, 143154.
Capuco, AV, Li, M, Long, E, Ren, S, Hruska, KS, Schorr, K and Furth, PA 2002b. Concurrent pregnancy retards mammary involution: effects on apoptosis and proliferation of mammary epithelium after forced weaning of mice. Biology of Reproduction 66, 14711476.
Capuco, AV, Ellis, SE, Hale, SA, Long, E, Erdman, RA, Zhao, X and Paape, MJ 2003. Lactation persistency: insights from mammary cell proliferation studies. Journal of Animal Science 81, 1831.
Clarke, R 2000. Introduction and overview: sex steroids in the mammary gland. Journal of Mammary Gland Biology and Neoplasia 5, 245250.
Connor, EE, Meyer, MJ, Li, RW, Van Amburgh, ME, Boisclair, YR and Capuco, AV 2007. Regulation of gene expression in the bovine mammary gland by ovarian steroids. Journal of Dairy Science 90, E55E65.
Dahl, GE, Buchanan, BA and Tucker, HA 2000. Photoperiodic effects on dairy cattle: a review. Journal of Dairy Science 83, 885893.
Dahl, GE, Elsasser, TH, Capuco, AV, Erdman, RA and Peters, RR 1997. Effects of a long daily photoperiod on milk yield and circulating concentrations of insulin-like growth factor-1. Journal of Dairy Science 80, 27842789.
Delbecchi, L, Miller, N, Prud’homme, C, Petitclerc, D, Wagner, G and Lacasse, P 2005. 17beta-Estradiol reduces milk synthesis and increases stanniocalcin gene expression in the mammary gland of lactating cows. Livestock Production Science 98, 5766.
Denamur, R and Martinet, J 1961. [Effect of hypophysectomy and pituitary stalk section on gestation in the sheep]. Annal of Endocrinology 22, 755759.
Deome, KB, Faulkin, LJ Jr, Bern, HA and Blair, PB 1959. Development of mammary tumors from hyperplastic alveolar nodules transplanted into gland-free mammary fat pads of female C3H mice. Cancer Research 19, 515520.
Dessauge, F, Finot, L, Wiart, S, Aubry, JM and Ellis, SE 2009. Effects of ovariectomy in prepubertal goats. Journal of Physiology and Pharmacology 60, 127133.
Dessauge, F, Lollivier, V, Ponchon, B, Bruckmaier, R, Finot, L, Wiart, S, Cutullic, E, Disenhaus, C, Barbey, S and Boutinaud, M 2011. Effects of nutrient restriction on mammary cell turnover and mammary gland remodeling in lactating dairy cows. Journal of Dairy Science 94, 46234635.
Dutta, U and Pant, K 2008. Aromatase inhibitors: past, present and future in breast cancer therapy. Medecine Oncology 25, 113124.
Ellis, SE, McFadden, TB and Akers, RM 1998. Prepubertal ovine mammary development unaffected by ovariectomy. Domestic Animal Endocrinology 15, 217225.
Elsasser, TH, Rumsey, TS and Hammond, AC 1989. Influence of diet on basal and growth hormone-stimulated plasma concentrations of IGF-I in beef cattle. Journal of Animal Science 67, 128141.
Flint, AP, Sheldrick, EL, Theodosis, DT and Wooding, FB 1986. Ovarian peptides: role of luteal oxytocin in the control of estrous cyclicity in ruminants. Journal of Animal Science 62 (suppl. 2), 6271.
Flint, DJ and Knight, CH 1997. Interactions of prolactin and growth hormone (GH) in the regulation of mammary gland function and epithelial cell survival. Journal of Mammary Gland Biology and Neoplasia 2, 4148.
Forde, N, Beltman, ME, Lonergan, P, Diskin, M, Roche, JF and Crowe, MA 2011. Oestrous cycles in Bos taurus cattle. Animal Reproduction Science 124, 163169.
Green, KA and Streuli, CH 2004. Apoptosis regulation in the mammary gland. Cell and Molecular Life Science 61, 18671883.
Hale, SA, Capuco, AV and Erdman, RA 2003. Milk yield and mammary growth effects due to increased milking frequency during early lactation. Journal of Dairy Science 86, 20612071.
Haslam, SZ and Woodward, TL 2001. Reciprocal regulation of extracellular matrix proteins and ovarian steroid activity in the mammary gland. Breast Cancer Research 3, 365372.
Hoshino, K 1978. Mammary transplantation and its histogenesis in mice. In Physiology of mammary gland (ed. A Yokoyama, H Mizuno and H Nagasawa), pp. 163228. University Park Press, Tokyo.
Hovey, RC, McFadden, TB and Akers, RM 1999. Regulation of mammary gland growth and morphogenesis by the mammary fat pad: a species comparison. Journal of Mammary Gland Biology and Neoplasia 4, 5368.
Hurley, WL 1989. Symposium: mammary gland function during involution and the declining phase of lactation. Journal of Dairy Science 72, 16371646.
Huynh, HT, Robitaille, G and Turner, JD 1991. Establishment of bovine mammary epithelial cells (MAC-T): an in vitro model for bovine lactation. Experimental and Cellular Research 197, 191199.
Janowski, T, Zdunczyk, S, Malecki-Tepicht, J, Baranski, W and Ras, A 2002. Mammary secretion of oestrogens in the cow. Domestical Animal Endocrinology 23, 125137.
Knight, CH and Peaker, M 1982. Development of the mammary gland. Journal of Reproduction and Fertility 65, 521536.
Knight, CH and Peaker, M 1984. Mammary development and regression during lactation in goats in relation to milk secretion. Quarterly Journal of Experimental Physiology 69, 331338.
Kratochwil, K 1971. In vitro analysis of the hormonal basis for the sexual dimorphism in the embryonic development of the mouse mammary gland. Journal of Embryology and Experimental Morphology 25, 141153.
Labussière, J, Marnet, PG, Combaud, JF, Beaufils, M and de la Chevalerie, FA 1993. Influence du nombre de corps jaunes sur la libération d'ocytocine lutéale, le transfert du lait alvéolaie dans la citerne et la production laitière chez la brebis. Reproduction Nutrition Development 33, 383393.
Lamote, I, Meyer, E, Massart-Leen, AM and Burvenich, C 2004. Sex steroids and growth factors in the regulation of mammary gland proliferation, differentiation, and involution. Steroids 69, 145159.
Linzell, JL 1973. Innate seasonal oscillations in the rate of milk secretion in goats. Journal of Physiology 230, 225233.
Long, E, Capuco, AV, Wood, DL, Sonstegard, T, Tomita, G, Paape, MJ and Zhao, X 2001. Escherichia coli induces apoptosis and proliferation of mammary cells. Cell Death and Differentiation 8, 808816.
Lonning, PE 2004. Aromatase inhibitors in breast cancer. Endocrine Related Cancer 11, 179189.
Marcek, JM and Swanson, LV 1984. Effect of photoperiod on milk production and prolactin of Holstein dairy cows. Journal of Dairy Science 67, 23802388.
Meyer, MJ, Capuco, AV, Boisclair, YR and Van Amburgh, ME 2006. Estrogen-dependent responses of the mammary fat pad in prepubertal dairy heifers. Journal of Endocrinology 190, 819827.
Miller, AR, Stanisiewski, EP, Erdman, RA, Douglass, LW and Dahl, GE 1999. Effects of long daily photoperiod and bovine somatotropin (Trobest) on milk yield in cows. Journal of Dairy Science 82, 17161722.
Miller, N, Delbecchi, L, Petitclerc, D, Wagner, GF, Talbot, BG and Lacasse, P 2006. Effect of stage of lactation and parity on mammary gland cell renewal. Journal of Dairy Science 89, 46694677.
Miller, WL 2007. Steroidogenic acute regulatory protein (StAR), a novel mitochondrial cholesterol transporter. Biochimica and Biophysica Acta 1771, 663676.
Mollett, TA, Erb, RE, Monk, EL and Malven, PV 1976. Changes in estrogen, progesterone, prolactine and lactation traits associated with injection of estradiol-17beta and progesterone into lactating cows. Journal of Dairy Science 42, 655663.
Morrissey, AD, Cameron, AWN and Tilbrook, AJ 2008. Artificial lighting during winter increases milk yield in dairy ewes. Journal of Dairy Science 91, 42384243.
Norgaard, JV, Sorensen, MT, Theil, PK, Sehested, J and Sejrsen, K 2008. Effect of pregnancy and feeding level on cell turnover and expression of related genes in the mammary tissue of lactating dairy cows. Animal 2, 588594.
Patel, OV, Takenouchi, N, Takahashi, T, Hirako, M, Sasaki, N and Domeki, I 1999. Plasma oestrone and oestradiol concentrations throughout gestation in cattle: relationship to stage of gestation and fetal number. Research in Veterinary Science 66, 129133.
Peters, RR, Chapin, LT, Emery, RS and Tucker, HA 1981. Milk yield, feed intake, prolactin, growth hormone, and glucocorticoid response of cows to supplemented light. Journal of Dairy Science 64, 16711678.
Petz, LN, Ziegler, YS, Schultz, JR, Kim, H, Kemper, JK and 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, 113122.
Purup, S, Sejrsen, K and Akers, RM 1995. Effect of bovine GH and ovariectomy on mammary tissue sensitivity to IGF-I in prepubertal heifers. Journal of Endocrinology 144, 153158.
Purup, S, Sejrsen, K, Foldager, J and 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, 1926.
Ray, EW, Averill, SC, Lyons, WR and Johnson, RE 1955. Rat placental hormonal activities corresponding to those of pituitary mammotropin. Endocrinology 56, 359373.
Schams, D, Kohlenberg, S, Amselgruber, W, Berisha, B, Pfaffl, MW and Sinowatz, F 2003. Expression and localisation of oestrogen and progesterone receptors in the bovine mammary gland during development, function and involution. Journal of Endocrinol 177, 305317.
Schutz, MM, Hansen, LB, Steuernagel, GR and Kuck, AL 1990. Variation of milk, fat, protein, and somatic cells for dairy cattle. Journal of Dairy Science 73, 484493.
Simpson, ER 2000. Biology of aromatase in the mammary gland. Journal of Mammary Gland Biology and Neoplasia 5, 251258.
Singh, K, Davis, SR, Dobson, JM, Molenaar, AJ, Wheeler, TT, Prosser, CG, Farr, VC, Oden, K, Swanson, KM, Phyn, CVC, Hyndman, DL, Wilson, T, Henderson, HV and Stelwagen, K 2008. cDNA microarray analysis reveals that antioxidant and immune genes are upregulated during involution of the bovine mammary gland. Journal of Dairy Science 91, 22362246.
Sobolewska, A, Motyl, T and Gajewska, M 2011. Role and regulation of autophagy in the development of acinar structures formed by bovine BME-UV1 mammary epithelial cells. European Journal of Cell Biology 90, 854864.
Sobolewska, A, Gajewska, M, Zarzynska, J, Gajkowska, B and Motyl, T 2009. IGF-I, EGF, and sex steroids regulate autophagy in bovine mammary epithelial cells via the mTOR pathway. European Journal of Cell Biology 88, 117130.
Sölkner, J and Fuchs, W 1987. A comparison of different measures of persistency with special respect to variation of test-day milk yields. Livestock Production Science 16, 305319.
Sorensen, A and Knight, CH 2002. Endocrine profiles of cows undergoing extended lactation in relation to the control of lactation persistency. Domestic Animal Endocrinology 23, 111123.
Stefanon, B, Colitti, M, Gabai, G, Knight, CH and Wilde, CJ 2002. Mammary apoptosis and lactation persistency in dairy animals. Journal of Dairy Research 69, 3752.
Svennersten-Sjaunja, K and Olsson, K 2005. Endocrinology of milk production. Domestic Animal Endocrinology 29, 241258.
Tremblay, G, Bernier-Dodier, P, Delbecchi, L, Wagner, GF, Talbot, BG and Lacasse, P 2009. Local control of mammary involution: is stanniocalcin-1 involved? Journal of Dairy Science 92, 19982006.
Veltmaat, JM, Mailleux, AA, Thiery, JP and Bellusci, S 2003. Mouse embryonic mammogenesis as a model for the molecular regulation of pattern formation. Differentiation 71, 117.
Wallace, C 1953. Observations on mammary development in calves and lambs. Journal of Agricultural Science 43, 413421.
Welty, FK, Smith, KL and Schanbacher, FL 1976. Lactoferrin concentration during involution of the bovine mammary gland. Journal of Dairy Science 59, 224231.
Wiltbank, M, Lopez, H, Sartori, R, Sangsritavong, S and Gumen, A 2006. Changes in reproductive physiology of lactating dairy cows due to elevated steroid metabolism. Theriogenology 65, 1729.
Woodward, TL 1991. Effects of ovarian steroids on bovine mammary epithelial cells: in vitro and in vivo evidence of indirect stimulation of proliferation. Virginia State University, Blacksburg Virginia.
Woodward, TL, Beal, WE and Akers, RM 1993. Cell interactions in initiation of mammary epithelial proliferation by oestradiol and progesterone in prepubertal heifers. Journal of Endocrinol 136, 149157.
Yart, L, Finot, L, Marnet, PG and Dessauge, F 2012a. Suppression of ovarian secretions before puberty strongly affects mammogenesis in the goat. Journal of Dairy Research 79, 157167.
Yart, L, Dessauge, F, Finot, L, Barbey, S, Marnet, PG and Lollivier, V 2012b. Ovariectomy improves lactation persistency in dairy cows. Journal of Dairy Science 95, 37943802.
Yart, L, Finot, L, Lollivier, V and Dessauge, F 2013a. Oestradiol enhances apoptosis in bovine mammary epithelial cells in vitro. The Journal of dairy research 80, 113121.
Yart, L, Lollivier, V, Finot, L, Dupont, J, Wiart, S, Boutinaud, M, Marnet, PG and Dessauge, F 2013b. Changes in mammary secretory tissue during lactation in ovariectomized dairy cows. Steroids 78, 973981.
Zarzynska, J, Gajewska, M and Motyl, T 2005. Effects of hormones and growth factors on TGF-beta1 expression in bovine mammary epithelial cells. Journal of Dairy Research 72, 3948.
Zhou, Y, Akers, RM and Jiang, H 2008. Growth hormone can induce expression of four major milk protein genes in transfected MAC-T cells. Journal of Dairy Science 91, 100108.

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