Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-24T07:40:43.492Z Has data issue: false hasContentIssue false

Mammary gland secretion: hormonal coordination of endocytosis and exocytosis

Published online by Cambridge University Press:  17 August 2009

S. Truchet
Affiliation:
INRA, UR1196 Génomique et Physiologie de la Lactation, F78352 Jouy-en-Josas, France
M. Ollivier-Bousquet*
Affiliation:
INRA, UR1196 Génomique et Physiologie de la Lactation, F78352 Jouy-en-Josas, France
Get access

Abstract

The mammary epithelium coordinates the uptake of milk precursors and the transport of milk components in order to produce milk of relatively constant composition at a particular stage of lactation, as long as the mammary gland is healthy. The mammary epithelial cell controls the uptake of blood-borne molecules at its basal side and the release of products into milk at its apical side, through mechanisms of internalization (endocytosis) and mechanisms of release (exocytosis). These events are strictly dependent on the physiological stage of the mammary gland. This review addresses the mechanisms responsible for these processes and points out new questions that remain to be answered concerning possible interconnections between them, for an optimal milk secretion.

Type
Full Paper
Copyright
Copyright © The Animal Consortium 2009

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, MR, Bauman, DE, Goodman, GT, Capuco, AV, Tucker, HA 1981. Prolactin regulation of cytological differentiation of mammary epithelial cells in periparturient cows. Endocrinology 109, 3140.CrossRefGoogle ScholarPubMed
Anantamongkol, U, Takemura, H, Suthiphongchai, T, Krishnamra, N, Horio, Y 2007. Regulation of Ca2+ mobilization by prolactin in mammary gland cells: possible role of secretory pathway Ca2+-ATPase type 2. Biochemical and Biophysical Research Communications 352, 537542.CrossRefGoogle ScholarPubMed
Boisgard, R, Chanat, E, Lavialle, F, Pauloin, A, Ollivier-Bousquet, M 2001. Roads taken by milk proteins in mammary epithelial cells. Livestock Production Science 70, 4961.CrossRefGoogle Scholar
Castino, R, Delpal, S, Bouguyon, E, Demoz, M, Isidoro, C, Ollivier-Bousquet, M 2008. Prolactin promotes the secretion of active cathepsin D at the basal side of rat mammary acini. Endocrinology 149, 40954105.CrossRefGoogle ScholarPubMed
Cho, JY, Léveillé, R, Kao, R, Rousset, B, Parlow, AF, JrBurak, WE, Mazzaferri, EL, Jhiang, SM 2000. Hormonal regulation of radioiodide uptake activity and NA+/I symporter expression in mammary glands. The Journal of Clinical Endocrinology and Metabolism 85, 29362943.Google ScholarPubMed
Darios, F, Davletov, B 2006. Omega-3 and omega-6 fatty acids stimulate cell membrane expansion by acting on syntaxin 3. Nature 440, 813817.CrossRefGoogle ScholarPubMed
Devinoy, E, Stinnakre, MG, Lavialle, F, Thépot, D, Ollivier-Bousquet, M 1995. Intracellular routing and release of caseins and growth hormone produced into milk from transgenic mice. Experimental Cell Research 221, 272280.CrossRefGoogle ScholarPubMed
Djonov, V, Andres, AC, Ziemiecki, A 2001. Vascular remodelling during the normal and malignant life cycle of the mammary gland. Microscopy Research and Technique 52, 182189.3.0.CO;2-M>CrossRefGoogle ScholarPubMed
Franke, WW, Lüder, MR, Kartenbeck, J, Zerban, H, Keenan, TW 1976. Involvement of vesicle coat material in casein secretion and surface regeneration. The Journal of Cell Biology 69, 173195.CrossRefGoogle ScholarPubMed
Geppert, M, Südhof, TC 1998. RAB3 and synaptotagmin: the yin and the yang of synaptic membrane fusion. Annual Review of Neuroscience 21, 7595.CrossRefGoogle Scholar
Gundelfinger, ED, Kessels, MM, Qualmann, B 2003. Temporal and spatial coordination of exocytosis and endocytosis. Nature Reviews Molecular Cell Biology 4, 127139.CrossRefGoogle ScholarPubMed
Handel, SE, Rennison, ME, Wilde, CJ, Burgoyne, RD 1991. Annexin II (calpactin I) in the mouse mammary gland: immunolocalisation by light-and electron microscopy. Cell and Tissue Research 264, 549554.Google Scholar
Haney, PM 2001. Localization of the glut1 glucose transporter to brefeldin A-sensitive vesicles of differentiated CIT3 mouse mammary epithelial cells. Cell Biology International 25, 277288.CrossRefGoogle ScholarPubMed
Herzog, V, Farquhar, MG 1977. Luminal membrane retrieved after exocytosis reaches most Golgi cisternae in secretory cells. Proceedings of the National Academy of Sciences of the United States of America 74, 50735077.CrossRefGoogle ScholarPubMed
Hue-Beauvais, C, Péchoux, C, Bouguyon, E, Chat, S, Truchet, S, Pauloin, A, Le Gouar, Y, Ollivier-Bousquet, M 2007. Localisation of caveolin in mammary tissue depends on cell type. Cell and Tissue Research 328, 521536.CrossRefGoogle ScholarPubMed
Keenan, TW 2001. Milk lipid globules and their surrounding membrane: a brief history and perspectives for future research. Journal of Mammary Gland Biology and Neoplasia 6, 365371.CrossRefGoogle ScholarPubMed
Kelleher, SL, Lönnerdal, B 2003. Marginal maternal Zn intake in rats alters mammary gland Cu transporter levels and milk Cu concentration and affects neonatal Cu metabolism. Journal of Nutrition 133, 21412148.CrossRefGoogle ScholarPubMed
Kelleher, SL, Lönnerdal, B 2005. Zip3 plays a major role in zinc uptake into mammary epithelial cells and is regulated by prolactin. American Journal of Physiology. Cell Physiology 288, C1042C1047.Google Scholar
Kelleher, SL, Lönnerdal, B 2006. Mammary gland copper transport is stimulated by prolactin through alterations in Ctr1 and Atp7A localization. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 291, R1181R1191.Google Scholar
Latham, CF, Osborne, SL, Cryle, MJ, Meunier, FA 2007. Arachidonic acid potentiates exocytosis and allows neuronal SNARE complex to interact with Munc18a. Journal of Neurochemistry 100, 15431554.CrossRefGoogle ScholarPubMed
Linzell, JL, Peaker, M 1971. Mechanism of milk secretion. Physiological Reviews 51, 564597.Google Scholar
Lkhider, M, Petridou, B, Aubourg, A, Ollivier-Bousquet, M 2001. Prolactin signalling to milk protein secretion but not to gene expression depends on the integrity of the Golgi region. Journal of Cell Science 114, 18831891.CrossRefGoogle Scholar
Llanos, RM, Michalczyk, AA, Freestone, DJ, Currie, S, Linder, MC, Ackland, ML, Mercer, JFB 2008. Copper transport during lactation in transgenic mice expressing the human ATP7A protein. Biochemical and Biophysical Research Communications 372, 613617.CrossRefGoogle ScholarPubMed
Lollivier, V, Marnet, PG, Delpal, S, Rainteau, D, Achard, C, Rabot, A, Ollivier-Bousquet, M 2006. Oxytocin stimulates secretory processes in lactating rabbit mammary epithelial cells. The Journal of Physiology 570, 125140.CrossRefGoogle ScholarPubMed
Lönnerdal, B 2007. Trace element transport in the mammary gland. Annual Review of Nutrition 27, 165177.CrossRefGoogle ScholarPubMed
Lutsenko, S, LeShane, ES, Shinde, U 2007. Biochemical basis of regulation of human copper-transporting ATPases. Archives of Biochemistry and Biophysics 463, 134148.CrossRefGoogle ScholarPubMed
Madon, RJ, Martin, S, Davies, A, Fawcett, HAC, Flint, DJ, Baldwin, SA 1990. Identification and characterization of glucose transport proteins in plasma membrane – and Golgi vesicle – enriched fractions prepared from lactating rat mammary gland. Biochemical Journal 272, 99105.CrossRefGoogle ScholarPubMed
Mamillapalli, R, VanHouten, J, Zawalich, W, Wysolmerski, J 2008. Switching of G-protein usage by the calcium-sensing receptor reverses its effect on parathyroid hormone-related protein secretion in normal versus malignant breast cells. The Journal of Biological Chemistry 283, 2443524447.Google Scholar
McShane, MP, Zerial, M 2008. Survival of the weakest: signaling aided by endosomes. Journal of Cell Biology 182, 823825.CrossRefGoogle ScholarPubMed
Meldolesi, J 1974. Dynamics of cytoplasmic membranes in Guinea pig pancreatic acinar cells. Journal of Cellular Biology 61, 113.CrossRefGoogle ScholarPubMed
Min, L, Leung, YM, Tomas, A, Watson, RT, Gaisano, HY, Halban, PA, Pessin, JE, Hou, JC 2007. Dynamin is functionally coupled to insulin granule exocytosis. The Journal of Biological Chemistry 282, 3353033536.CrossRefGoogle ScholarPubMed
Monks, J, Neville, MC 2004. Albumin transcytosis across the epithelium of the lactating mouse mammary gland. The Journal of Physiology 560, 267280.CrossRefGoogle ScholarPubMed
Nemeth, BA, Tsang, SWY, Geske, RS, Haney, PM 2000. Golgi targeting of the GLUT1 glucose transporter in lactating mouse mammary gland. Pediatric Research 47, 444450.CrossRefGoogle ScholarPubMed
Neville, MC, Peaker, M 1979. The secretion of calcium and phosphorus into milk. Journal of Physiology (London) 290, 5967.CrossRefGoogle ScholarPubMed
Nickerson, SC, Keenan, TW 1979. Distribution and orientation of microtubules in milk secreting epithelial cells of rat mammary gland. Cell and Tissue Research 202, 303312.CrossRefGoogle ScholarPubMed
Ollivier-Bousquet, M 1978. Early effect of prolactin on lactating rabbit mammary gland. Cell and Tissue Research 187, 2543.CrossRefGoogle ScholarPubMed
Ollivier-Bousquet, M 1979. Effet de la cytochalasine B et de la colchicine sur l’action rapide de la prolactine dans la glande mammaire de lapin. European Journal of Cellular Biology 19, 168174.Google Scholar
Ollivier-Bousquet, M 1983. Rôle du Ca2+ dans la sécrétion des caséines du lait par la cellule épithéliale mammaire de lapine en lactation. Biologie Cellulaire 49, 127136.Google Scholar
Ollivier-Bousquet, M 1993. Les hormones du lait : provenance et rôles. INRA Productions Animales 6, 253263.CrossRefGoogle Scholar
Ollivier-Bousquet, M 1998. Transferrin and prolactin transcytosis in lactating mammary epithelial cell. Journal of Mammary Gland Biology and Neoplasia 3, 303313.Google Scholar
Ollivier-Bousquet, M 2002. Milk lipid and protein traffic in mammary epithelial cells: joint and independent pathways. Reproduction Nutrition Development 42, 149162.Google Scholar
Ollivier-Bousquet, M, Denamur, R 1973. Inhibition par la colchicine de la sécrétion des protéines du lait. Comptes Rendus de l’Académie des Sciences de Paris 276, 21832186.Google Scholar
Ollivier-Bousquet, M, Devinoy, E 2005. Physiology of lactating: old questions, new approaches. Livestock Production Science 98, 163173.CrossRefGoogle Scholar
Ollivier-Bousquet, M, Radwanyi, F, Bon, C 1991. Crotoxin, a phospholipase A2 neurotoxin from snake venom, interacts with epithelial mammary cells, is internalized and induces secretion. Molecular and Cellular Endocrinology 82, 4150.CrossRefGoogle ScholarPubMed
Patton, S 1976a. Structure and function of mammary epithelium. In Biomedical aspects of lactation (ed. S Patton and RG Jensen), pp. 2250. Pergamon Press, Oxford, New York.Google Scholar
Patton, S 1976b. Mechanisms of secretion: effects of colchicine and vincristine on composition and flow of milk in the goat. Journal of Dairy Science 59, 14141419.CrossRefGoogle ScholarPubMed
Pitelka, DR, Hamamoto, ST 1983. Ultrastructure of the mammary secretory cell. In Biochemistry of lactation (ed. TB Mephan), pp. 2970. Elsevier Science Publishers, Amsterdam.Google Scholar
Rickman, C, Davietov, B 2005. Arachidonic acid allows SNARE complex formation in the presence of Munc18. Chemistry and Biology 12, 545553.CrossRefGoogle ScholarPubMed
Riskin, A, Nannegari, VH, Mond, Y 2008. Acute effectors of GLUT1 glucose transporter subcellular targeting in CIT3 mouse mammary epithelial cells. Pediatric Research 63, 5661.CrossRefGoogle ScholarPubMed
Rohrbough, J, Broadie, K 2005. Lipid regulation of the synaptic vesicle cycle. Nature Reviews Neuroscience 6, 139150.CrossRefGoogle ScholarPubMed
Ryan, TA 2006. A pre-synaptic to-do list for coupling exocytosis to endocytosis. Current Opinion in Cell Biology 18, 416421.CrossRefGoogle ScholarPubMed
Selvaraj, NG, Omi, E, Gibori, G, Rao, MC 2000. Janus kinase 2 (JAK2) regulates prolactin-mediated chloride transport in mouse mammary epithelial cells through tyrosine phosphorylation of Na+-K+-2Cl cotransporter. Molecular Endocrinology 14, 20542065.Google Scholar
Shennan, DB, Peaker, M 2000. Transport of milk constituents by the mammary gland. Physiological Reviews 80, 925951.Google Scholar
Vadlamudi, RK, Wang, RA, Talukder, AH, Adam, L, Johnson, R, Kumar, R 2000. Evidence of Rab3A expression, regulation of vesicle trafficking, and cellular secretion in response to heregulin in mammary epithelial cells. Molecular and Cellular Biology 20, 90929101.Google Scholar
VanHouten, JN, Neville, MC, Wysolmerski, JJ 2007. The calcium-sensing receptor regulates plasma membrane calcium adenosine triphosphatase isoform 2 activity in mammary epithelial cells: a mechanism for calcium-regulated calcium transport into milk. Endocrinology 148, 59435954.CrossRefGoogle ScholarPubMed
VanHouten, JN, Wysolmerski, JJ 2007. Transcellular calcium transport in mammary epithelial cells. Journal of Mammary Gland Biology and Neoplasia 12, 223235.Google Scholar
Varghese, B, Barrière, H, Carbone, CJ, Banerjee, A, Swaminathan, G, Plotnikov, A, Xu, P, Peng, J, Goffin, V, Lukacs, GG, Fuchs, SY 2008. Polyubiquitination of prolactin receptor stimulates its internalization, postinternalization sorting, and degradation via the lysosomal pathway. Molecular and Cellular Biology 28, 52755287.Google Scholar
Verhage, M 2005. Fatty acids and grease to exocytosis. Chemistry and Biology 12, 511512.CrossRefGoogle ScholarPubMed
Vilotte, JL, Whitelaw, CBA, Ollivier-Bousquet, M, Shennan, DB 2003. Biosynthesis of milk proteins. In Advanced dairy chemistry (ed. PF Fox and LH McSweeney), vol. 1, pp. 699738. Kluwer Academic/Plenum Publishers, New York, USA.Google Scholar
Wang, CC, Shi, H, Guo, K, Ng, CP, Li, J, Gan, BQ, Liew, HC, Leinomen, J, Rajaniemi, H, Zhou, ZH, Zeng, Q, Hong, W 2007. VAMP8/Endobrevin as a general vesicular SNARE for regulated exocytosis of the exocrine system. Molecular Biology of the Cell 18, 10561063.Google Scholar
Zhang, P, Sawicki, V, Lewis, A, Hanson, L, Monks, J, Neville, MC 2000. The effect of serum iron concentration on iron secretion into mouse milk. The Journal of Physiology 522, 479491.CrossRefGoogle ScholarPubMed
Zhao, FQ, Keating, AF 2007. Expression and regulation of glucose transporters in the bovine mammary gland. Journal of Dairy Sciences 90, E76E86.Google Scholar