Review

Prolactin and Other Hormones:Synergistic Action on Regulating Milk Composition Synthesis in Mammary Glands

  • SHENG Ran ,
  • YAN Sumei
Expand
  • College of Animal Science, Inner Mongolia Agriculture University, Huhhot 010018, China

Received date: 2013-12-23

  Online published: 2014-05-30

Abstract

Prolactin plays clear and established roles in regulating the growth of mammary gland, galactosis, milk secretion and milk component synthesis; in most cases, prolactin regulates mammary gland functions synergistically with other hormones including estrogen, progestogen, glucocorticoid and insulin. This paper reviewed the progress in regulation of synergistic action between prolactin and other hormones on milk component synthesis in mammary glands, providing advisable references for further study on mechanism of milk component synthesis in mammary gland.

Cite this article

SHENG Ran , YAN Sumei . Prolactin and Other Hormones:Synergistic Action on Regulating Milk Composition Synthesis in Mammary Glands[J]. Chinese Journal of Animal Nutrition, 2014 , 26(6) : 1435 -1443 . DOI: 10.3969/j.issn.1006-267x.2014.06.003

References

[1] TROTT J F,VONDERHAAR B K,HOVEY R C.Historical perspectives of prolactin and growth hormone as mammogens,lactogens and galactagogues-agog for the future[J].Journal of Mammary Gland Biology and Neoplasia,2008,13(1):3-11.  
[2] FREEMAN M E,KANYICSKA B,LERANT A,et al.Prolactin:structure,function,and regulation of secretion[J].Physiological Reviews,2000,80(4):1523-1631.
[3] CLAPP C,THEBAULT S,MARTINEZ DE L E G.Role of prolactin and vasoinhibins in the regulation of vascular function in mammary gland[J].Journal of Mammary Gland Biology and Neoplasia,2008,13(1):55-67.  
[4] CORBACHO A M,MARTINEZ DE L E,CLAPP C.Roles of prolactin and related members of the prolactin/growth hormone/placental lactogen family in angiogenesis[J].The Journal of Endocrinology,2002,173(2):219-238.  
[5] 谭敦勇,彭湘萍.催乳素受体研究[J].生理科学进展,2012,40(1):17-23.
[6] CLEVENGER C V,CHANG W P,NGO W,et al.Expression of prolactin and prolactin receptor in human breast carcinoma.Evidence for an autocrine/paracrine loop[J].The American Journal of Pathology,1995,146(3):695-705.
[7] HOVEY R C,ASAI-SATO M,WARRI A,et al.Effects of neonatal exposure to diethylstilbestrol,tamoxifen,and toremifene on the BALB/c mouse mammary gland[J].Biology of Reproduction,2005,72(2):423-435.  
[8] BRISKEN C,KAUR S,CHAVARRIA T E,et al.Prolactin controls mammary gland development via direct and indirect mechanisms[J].Developmental Biology,1999,210(1):96-106.  
[9] FARMER C,PALIN M F.Exogenous prolactin stimulates mammary development and alters expression of prolactin-related genes in prepubertal gilts[J].Journal of Animal Science,2005,83(4):825-832.
[10] HOVEY R C,TROTT J F,GINSBURG E,et al.Transcriptional and spatiotemporal regulation of prolactin receptor mRNA and cooperativity with progesterone receptor function during ductal branch growth in the mammary gland[J].Developmental Dynamic,2001,222(2):192-205.  
[11] FREEMAN M E,KANYICSKA B,LERANT A,et al.Prolactin:structure,function,and regulation of secretion[J].Physiological Reviews,2000,80(4):1523-1531.
[12] HORSEMAN N D.Prolactin and mammary gland development[J].Journal of Mammary Gland Biology and Neoplasia,1999,4(1):79-88.  
[13] NEVILLE M C,MCFADDEN T B,FORSYTH I.Hormonal regulation of mammary differentiation and milk secretion[J].Journal of Mammary Gland Biology and Neoplasia,2002,7(1):49-66.  
[14] 佟慧丽,高学军,李庆章.胰岛素、催乳素对奶山羊乳腺上皮细胞泌乳功能的影响[J].畜牧兽医学报,2008,39(6):721-725.
[15] FARMER C,ROBERT S,RUSHEN J.Bromocriptine given orally to periparturient of lactating sows inhibits milk production[J].Journal of Animal Science,1998,76(3):750-757.
[16] SMITH V G,BECK T W,CONVEY E M,et al.Bovine serum prolactin,growth hormone,cortisol and milk yield after ergocryptine[J].Neuroendocrinology,1974,15(3/4):172-181.
[17] LACASSE P,LOLLIVIER V,BRUCKMAIER R M,et al.Effect of the prolactin-release inhibitor quinagolide on lactating dairy cows[J].Journal of Dairy Science,2011,94(3):1302-1309.  
[18] FARMER C,SORENSEN M T,ROBERT S,et al.Administering exogenous porcine prolactin to lactating sows:milk yield,mammary gland composition,and endocrine and behavioral responses[J].Journal of Animal Science,1999,77(7):1851-1859.
[19] PLAUT K,BAUMAN D E,AGERGAARD N,et al.Effect of exogenous prolactin administration on lactational performance of dairy cows[J].Domestic Animal Endocrinology,1987,4(4):4279-4290.
[20] JACQUEMET N,PRIGGE E C.Effect of increased postmilking prolactin concentrations on lactation,plasma metabolites,and pancreatic hormones in lactating goats[J].Journal of Dairy Science,1991,74(1):109-114.  
[21] WALL E H,H.CRAWFORD H M,ELLIS S E,et al.Mammary response to exogenous prolactin or frequent milking during early lactation in dairy cows[J].Journal of Dairy Science,2006,89(12):4640-4648.  
[22] 杨建英,张勇法,王艳玲,等.大豆黄酮对奶牛产奶量和乳中常规成分的影响[J].饲料研究,2005(6):30-31.
[23] BEN-JONATHAN N,HUGO E R,BRANDEBOURG T D,et al.Focus on prolactin as a metabolic hormone[J].Trends in Endocrinology and Metabolism,2006,17(3):110-116.  
[24] 朱河水,王月影,王艳玲,等.大豆黄酮对奶牛泌乳性能及血浆中激素水平的影响[J].畜牧兽医科学,2006,22(5):20-22.
[25] HARRIS J,STANFORD P M,SUTHERLAND K,et al.Socs2 and elf5 mediate prolactin-induced mammary gland development[J].Molecular Endocrinology,2006,20(5):1177-1187.  
[26] ISMAIL P M,AMATO P,SOYAL S M,et al.Progesterone involvement in breast development and tumorigenesis-as revealed by progesterone receptor ‘knockout’and‘knockin’ mouse models[J].Steroids,2003,68(10/11/12/13):779-787.
[27] 江青东.大鼠乳腺发育过程中雌激素、孕激素、催乳素及其相应受体水平变化规律的研究[D].硕士学位论文.郑州:河南农业大学,2006:31-32.
[28] STOUDEMIRE G A,STUMPF W E,SAR M.Synergism between prolactin and ovarian hormones of DNA synthesis in rats mammary gland[J].Proceedings of the Society for Experimental Biology and Medicine,1975,149(1):189-192.  
[29] MULDOON T G.Interplay between estradiol and prolactin in the regulation of steroid hormone receptor levels,nature,and functionality in normal mouse mammary tissue[J].Endocrinology,1981,109(5):1339-1346.  
[30] TROTT J F,HORIGAN K C,GLOVICZKI J M,et al.Tissue-specific regulation of porcine prolactin receptor expression by estrogen,progesterone,and prolactin[J].The Journal of Endocrinology,2009,202(1):153-166.  
[31] 张少英.泌乳的激素调控[J].国外畜牧学:草食家畜,1990(1):31-35.
[32] 杨建英.大豆黄酮对不同泌乳期奶牛产奶量、乳成分的影响及相关作用机制的研究[D].硕士学位论文.郑州:河南农业大学,2003:27-28.
[33] GOODMAN G T,AKERS R M,FRIDERICI K H,et al.Hormonal regulation of alpha-lactalbumin secretion from bovine mammary tissue cultured in vitro[J]Endocrinology,1983,112(4):1324-1330.
[34] SCULLY K M,GLEIBERMAN A S,LINDZEY J,et al.Role of estrogen receptor-alpha in the anterior pituitary gland[J].Molecular Endocrinology,1997,11(6):674-681.
[35] FRASOR J,GIBORI G.Prolactin regulation of estrogen receptor expression[J].Trends in Endocrinology and Metabolism,2003,14(3):118-123.  
[36] GONZLEZ L,ZAMBRANO A,LAZARO-TRUEBA I,et al.Activation of the unliganded estrogen receptor by prolactin in breast cancer cells[J].Oncogene,2009,28(10):1298-1308.  
[37] GUTZMAN J H,NIKOLAI S E,RUQOWSKI D E,et al.Prolactin and estrogen enhance the activity of activating protein 1 in breast cancer cells:role of extracellularly regulated kinase 1/2-mediated signals to c-fos[J].Molecular Endocrinology,2005,19(7):1765-1778.  
[38] RASMUSSEN L M,FREDERIKSEN K S,DIN N,et al.Prolactin and oestrogen synergistically regulate gene expression and proliferation of breast cancer cells[J].Endocrine:Related Cancer,2010,17(3):809-822.  
[39] GUTZMAN J H,MILLER K K,SCHULER L A.Endogenous human prolactin and not exogenous human prolactin induces estrogen receptor alpha and prolactin receptor expression and increases estrogen responsiveness in breast cancer cells[J].The Journal of Steroid Biochemistry and Molecular Biology,2004,88(1):69-77.  
[40] DUAN R,GINSBURG E,VONDERHAAR B K.Estrogen stimulates transcription from the human prolactin distal promoter through AP1 and estrogen responsive elements in T47D human breast cancer cells[J].Molecular and Cellular Endocrinology,2008,281(1/2):9-18.
[41] ORMANDY C J,CAMUS A,BARRA J,et al.Null mutation of the prolactin receptor gene produces multiple reproductive defects in the mouse[J].Genes & Development,1997,11(2):167-178.  
[42] ACOSTA J J,MUNOZ R M,GONZALEZ L,et al.Src mediates prolactin-dependent proliferation of T47D and MCF7 cells via the activation of focal adhesion kinase/Erk1/2 and phosphatidylinositol 3-kinase pathways[J].Molecular Endocrinology,2003,17(11):2268-2282.  
[43] TAN D,JOHNSON D A,WU W,et al.Unmodified prolactin (PRL) and S179D PRL-initiated bioluminescence resonance energy transfer between homo- and hetero-pairs of long and short human PRL receptors in living human cells[J].Molecular Endocrinology,2005,19(5):1291-1303.  
[44] ALI S,EDERY M,PELLEGRINI I,et al.The Nb2 form of prolactin receptor is able to activate a milk protein gene promoter[J].Molecular Endocrinology,1992,6(8):1242-1248.
[45] BEN-JONATHAN N,LAPENSEE C R,LAPENSEE E W.What can we learn from rodents about prolactin in humans[J].Endocrine Reviews,2008,29(1):1-41.  
[46] VIRGO B B,BELLWARD G D.Serum progesterone levels in the pregnant and postpartum laboratory mouse[J].Endocrinology,1974,95(5):1486-1490.  
[47] LYDON J P,DEMAYO F J,FUNK C R,et al.Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities[J].Genes & Development,1995,9(18):2266-2278.  
[48] HORSEMAN N D,ZHAO W,MONTECINO-RODRIGUEZ E,et al.Defective mammopoiesis,but normal hematopoiesis,in mice with a targeted disruption of the prolactin gene[J].EMBO,1997,16(23):6926-6935.  
[49] OLIVER C H,WATSON C J.Making milk:a new link between STAT5 and Akt1[J].JAKSTAT,2013,2(2):e23228.
[50] EDERY M,MCGRATH M,LARSON L,et al.Correlation between in vitro growth and regulation of estrogen and progesterone receptors in rat mammary epithelial cells[J].Endocrinology,1984,115(5):1691-1697.  
[51] GRIMM S L,SEAGROVES T N,KABOTYANSKI E B,et al.Disruption of steroid and prolactin receptor patterning in the mammary gland correlates with a block in lobuloalveolar development[J].Molecular Endocrinology,2002,16(12):2675-2691.  
[52] HARAGUCHI S,GOOD R A,ENGELMAN R W,et al.Human prolactin regulates transfected MMTV LTR-directed gene expression in a human breast-carcinoma cell line through synergistic interaction with steroid hormones[J].International Journal of Cancer,1992,52(6):928-933.  
[53] MORABITO J E,TROTT J F,KORZ D M,et al.A 5’ distal palindrome within the mouse mammary tumor virus-long terminal repeat recruits a mammary gland-specific complex and is required for a synergistic response to progesterone plus prolactin[J].Journal of Molecular Endocrinology,2008,41(2):75-90.  
[54] SRIVASTAVA S,MATSUDA M,HOU Z,et al.Receptor activator of NF-kappaB ligand induction via Jak2 and Stat5a in mammary epithelial cells[J].The Journal Biological Chemistry,2003,278(46):46171-46178.  
[55] KEATING A F,DAVOREN P,SMITH T J,et al.Bovine kappa-casein gene promoter haplotypes with potential implications for milk protein expression[J].Journal of Dairy Science,2007,90(9):4092-4099.  
[56] LAU C,SULLIVAN M K,HAZELWOOD R L.Effects of diabetes mellitus on lactation in the rat[J].Proceedings of the Society for Experimental Biology Medicine,1993,204(1):81-89.  
[57] GRIINARI J M,MCGUIRE M A,DWYER D A,et al.The role of insulin in the regulation of milk protein synthesis in dairy cows[J].Journal of Dairy Science,1997,80(10):2361-2371.  
[58] MOLENTO C F,BLOCK E,CUE R I,et al.Effects of insulin,recombinant bovine somatotropin,and their interaction on insulin-like growth factor-Ⅰ secretion and milk protein production in dairy cows[J].Journal of Dairy Science,2002,85(4):738-747.  
[59] CHOI K M,BARASH I,RHOADS R E.Insulin and prolactin synergistically stimulate beta-casein messenger ribonucleic acid translation by cytoplasmic polyadenylation[J].Molecular Endocrinology,2004,18(7):1670-1686.  
[60] 王加启.胰岛素在多个水平调节奶牛乳腺乳蛋白质合成[J].奶业研究简报,2012(2):3.
[61] MENZIES K K,LEE H J,LEFVRE C,et al.Insulin,a key regulator of hormone responsive milk protein synthesis during lactogenesis in murine mammary explants[J].Functional & Integrative Genomics,2010,10(1):87-95.  
[62] MUSSO T,JOHNSTON J A,LINNEKIN D,et al.Regulation of JAK3 expression in human monocytes: phosphorylation in response to interleukins 2,4,and 7[J].The Journal of Experimental Medicine,1995,181(4):1425-1431.  
[63] ROSEN J M,WYSZOMIERSKI S L,HADSELL D.Regulation of milk protein gene expression[J].Annual Review of Nutrition,1999(19):407-436.
[64] 王皓宇,秦彤,郝海生,等.胰岛素对体外培养奶牛乳腺上皮细胞乳蛋白、乳脂肪合成相关基因mRNA表达的影响[J].畜牧兽医学报,2013,44(5):710-718.
[65] FERRON M,WEI J,YOSHIZAWA T,et al.Insulin signaling in osteoblasts integrates bone remodeling and energy metabolism[J].Cell,2010,142(2):296-308.  
[66] RHOADS R E,GRUDZIEN-NOGALSKA E.Translational regulation of milk protein synthesis at secretory activation[J].Journal of Mammary Gland Biology and Neoplasia,2007,12(4):283-292.  
[67] SMIRNOVA O V,OSTROUKHOVA T Y,BOGORAD R L.JAK-STAT pathway in carcinogenesis:is it relevant to cholangiocarcinoma progression[J].World Journal of Gastroenterology,2007,13(48):6478-6491.  
[68] BURGOS S A,DAI M,CANT J P.Nutrient availability and lactogenic hormones regulate mammary protein synthesis through the mammalian target of rapamycin signaling pathway[J].Journal of Dairy Science,2010,93(1):153-161.  
[69] 田青,季昀,庞学燕,等.胰岛素对奶牛乳腺上皮细胞酪蛋白合成调节机理的研究[J].动物营养学报,2013,25(3):550-560.
[73] 程光民,陈凤梅,林雪彦,等.葡萄糖和胰岛素同时灌注对奶山羊乳脂合成的影响[J].动物营养学报,2009,21(2):192-198.
[74] AKERS R M.Major advances associated with hormone and growth factor regulation of mammary growth and lactation in dairy cows[J].Journal of Dairy Science,2006,89(4):1222-1234.  
[75] CASEY T M,PLAUT K.The role of glucocorticoids in secretory activation and milk secretion,a historical perspective[J].Journal of Mammary Gland Biology and Neoplasia,2007,12(4):293-304.  
[76] DOPPLER W,WINDEGGER M,SORATROI C,et al.Expression level-dependent contribution of glucocorticoid receptor domains for functional interaction with STAT5[J].Molecular and Cellular Biology,2001,21(9):3266-3279.  
[77] STELWAGEN K,MCFADDEN H A,DEMMER J.Prolactin,alone or in combination with glucocorticoids,enhances tight junction formation and expression of the tight junction protein occludin in mammary cells[J].Molecular and Cellular Endocrinology,1999,156(1/2):55-61.
[78] BERTUCCI P Y,QUAGLINO A,POZZI A G,et al.Glucocorticoid-induced impairment of mammary gland involution is associated with STAT5 and STAT3 signaling modulation[J].Endocrinology,2010,151(12): 5730-5740.  
[79] HOUDEBINE L M,TEYSSOT B,DJIANE J,et al.Control of the expression of milk protein genes by prolactin,glucocorticoids and progesterone[J].Annales d’endocrinologie,1982,43(5):354-369.
[80] KABOTYANSKI E B,RIJNKELS M,FREEMAN-ZADROWSKI C,et al.Lactogenic hormonal induction of long distance interactions between beta-casein gene regulatory elements[J].The Journal of Biological Chemistry,2009,284(34):22815-22824.  
Outlines

/