Skip to main content
Log in

Secretory membranes of the lactating mammary gland

  • Published:
Protoplasma Aims and scope Submit manuscript

Summary

The lactating mammary gland is one of the most highly differentiated and metabolically active organs in the body. Membranes of the lactating mammary cell have important roles in transmitting from one membrane to another of hormonal information and in milk secretion, which is the final event. During milk secretion, the projection of the surface membrane into the alveolar lumen by enveloping intracellular lipid droplets with the apical plasma membrane is one of the most remarkable aspects of biological membrane action throughout nature.

This review focuses on current knowledge about membranes in the lactating mammary gland. (1) Advances in the isolation and properties of membranes, especially the plasma membrane and Golgi-derived secretory vesicles, concerned with milk secretion from the lactating mammary gland are described. (2) Milk serum components are secreted by fusing the membranes of secretory vesicles that condense milk secretions with the plasma membrane in the apical regions. This occurs through the formation of a tubular-shaped projection and vesicular depression in a ball-and-socket configuration, as well as by simple fusion. (3) Intracellular lipid droplets are directly extruded from the mammary epithelial cells by progressive envelopment of the plasma membranes in the apical regions. (4) The balance between the surface volume lost in enveloping lipid droplets and that provided by fusion of the secretory vesicle and other vesicles with the apical plasma membrane is discussed. (5) The membrane surrounding a milk fat globule, which is referred to as the milk fat globule membrane (MFGM), is composed of at least the coating membrane of an intracellular lipid droplet, of the apical plasma membrane and secretory vesicle membrane, and of a coat material. Consequently, MFGM is molecularly different from the plasma membrane in composition. (6) MFGM of bovine milk is structurally composed of an inner coating membrane and outer plasma membrane just after segregation. These two membranes are fused and reorganized through a process of vesiculation and fragmentation to stabilize the fat globules. Hypothetical structural models for MFGM from bovine milk fat globules just after secretion and after rearrangement are proposed.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

MFGM:

milk fat globule membrane

HEPES:

N-2-hydroxylpiperazine-N′-2-ethanesulfonic acid

INT:

2-(p-indophenyl)-3-(p-nitrophenyl)-5-phenyltetrazolium

SDS-PAGE:

polyacrylamide gel electrophoresis in the presence of sodium dodecyl sulfate

Sph:

sphingomyelin

PC:

phosphatidyl choline

PE:

phosphatidyl ethanolamine

PS:

phosphatidyl serine

PI:

phosphatidyl inositol

PAS:

periodic acid-Schiff reagent

CB:

Coomassie brilliant blue R-250

References

  • Amar-Costesec A, Wibo M, Thines-Sempoux D, Beaufay H, Berthet J (1974) Analytical study of microsomes and isolated subcellular membranes from rat liver. IV. Biochemical, physical and morphological modifications induced by digitonin, EDTA and pyrophosphate. J Cell Biol 62: 717–745

    Google Scholar 

  • Ahkong QF, Fisher D, Tampion W, Lucy JA (1975) Mechanism of cell fusion. Nature 253: 194–195

    Google Scholar 

  • Anderson M, Cawston TE (1975) Reviews of the progress of dairy science. The milk-fat globule membrane. J Dairy Res 42: 459–483

    Google Scholar 

  • Aronson NN Jr, Touster O (1974) Isolation of rat liver plasma membrane fragments in isotonic sucrose. Methods Enzymol 31: 90–102

    Google Scholar 

  • Bargmann W, Knoop A (1959) Über der Morphologie der Milchsekretion. Lichtund elektronenmikroskopische Studien an der Milchdrüse der Ratte. Z Zellforsch Mikrosk Anat 49: 344–388

    Google Scholar 

  • —, Fleischauer K, Knoop A (1959) Über die Morphologie der Milchsekretion. II. Zugleich eine Kritik am Schema der Sekretionsmorphologie. Z. Zellforsch Mikrosk Anat 53: 545–568

    Google Scholar 

  • Bauer H (1972) Ultrastructural observations on the milk fat globule envelop of cow's milk. J Dairy Sci 55: 1375–1387

    Google Scholar 

  • Baumrucker CR, Keenan TW (1974) Membranes of mammary gland: VIII. Isolation and composition of nuclei and nuclear membrane from bovine mammary gland. J Dairy Sci 57: 24–31

    Google Scholar 

  • — — (1975 a) Membranes of mammary gland. XI. Marker enzyme distribution profiles for membranous components from bovine mammary gland. J Dairy Sci 58: 1282–1287

    Google Scholar 

  • — — (1975 b) Membranes of mammary gland. X. Adenosine triphosphate dependent calcium accumulation by Golgi apparatus rich fractions from bovine mammary gland. Exp Cell Res 90: 253–260

    Google Scholar 

  • Beams HW, Kessel RG (1968) The Golgi apparatus: structure and function. Int Rev Cytol 23: 209–276

    Google Scholar 

  • Bell ML, Lazarus HM, Herman AH, Egdahl RH, Rutenburg AM (1971) pH dependent changes in cell membrane stability. Proc Soc Exp Biol Med 136: 298–299

    Google Scholar 

  • Bengtsson G, Olivecrona T (1982) Activation of lipoprotein lipase by apolipoprotein CII: demonstration of an effect of the activator on the binding of the enzyme to milk-fat globules. FEBS Lett 147: 183–187

    Google Scholar 

  • Berridge MJ (1984) Inositol triphosphate and diacylglycerol as second messengers. Biochem J 220: 345–360

    Google Scholar 

  • Bingham EW, Farrell HM Jr (1974) Casein kinase from the Golgi apparatus of lactating mammary gland. J Biol Chem 249: 3647–3651

    Google Scholar 

  • Bingham EW, Farrell HM Jr (1977) Phosphorylation of casein by the lactating mammary gland: a review. J Dairy Sci 60: 1199–1207

    Google Scholar 

  • — —, Basch JJ (1972) Phosphorylation of casein. Role of the Golgi apparatus. J Biol Chem 247: 8193–8194

    Google Scholar 

  • —, Groves ML (1979) Properties of casein kinase from lactating bovine mammary gland. J Biol Chem 254: 4510–4515

    Google Scholar 

  • Bruder G, Heid H, Jarasch E-D, Keenan TW, Mather IH (1982) Characteristics of membrane-bound and soluble forms of xanthine oxidase from milk and endothelial cells of capillaries. Biochim Biophys Acta 701: 357–369

    Google Scholar 

  • Buchheim W (1982) Paracrystalline arrays of milk fat globule membrane-associated proteins as revealed by freeze-fracture. Naturwissenschaften 69: 505–506

    Google Scholar 

  • —, Welsch U (1973) Evidence for the submicellar composition of casein micelles on the basis of electron microscopical studies. Neth Milk Dairy J 27: 163–180

    Google Scholar 

  • — —, Huston GE, Patton S (1988) Glycoprotein filament removal from human milk fat globules by heat treatment. Pediatrics 81: 141–146

    Google Scholar 

  • Cameron IL, Sparks RL, Seelig LL Jr (1980) Concentration of calcium and other elements at a subcellular level in the lactating epithelium of rat. Cytobios 27: 89–96

    Google Scholar 

  • Capasso JM, Keenan TW, Abeijon C, Hirschberg CB (1989) Mechanism of phosphorylation in the lumen of the Golgi apparatus. Translocation of ATP into Golgi vesicles from rat liver and mammary gland. J Biol Chem 264: 5233–5240

    Google Scholar 

  • Castle JD, Jamieson JD, Palade GE (1975) Secretion granules of the rabbit parotid gland. Isolation, subfractionation, and characterization of the membrane and content subfractions. J Cell Biol 64: 182–210

    Google Scholar 

  • Coffey RG, Reithel FJ (1968) The lactose synthetase particles of lactating bovine mammary gland. Characteristics of the particles. Biochem J 109: 177–183

    Google Scholar 

  • Davis CL, Bauman DE (1974) General metabolism associated with the synthesis of milk. In: Larson BL, Smith VR (eds) Lactation. A comprehensive treatise, vol 2. Academic Press, New York, pp 3–30

    Google Scholar 

  • Dean RT (1977) Lysosomes and membrane recycling: a hypothesis. Biochem J 168: 603–605

    Google Scholar 

  • De Duve C (1971) Tissue fractionation past and present. J Cell Biol 50: 20 D-55 D

    Google Scholar 

  • Deeney JT, Valivullah HM, Dapper CH, Dylewski DP, Keenan TW (1985) Microlipid droplets in milk secreting mammary epithelial cells: evidence that they originate from endoplasmic reticulum and are precursors of milk lipid globules. Eur J Cell Biol 38: 16–26

    Google Scholar 

  • De Pierre JW, Karnovsky ML (1973) Plasma membranes of mammalian cells. A review of methods of their characterization and isolation. J Cell Biol 56: 275–303

    Google Scholar 

  • Dowben RM, Brunner JR, Philpott DE (1967) Studies of milk fat globule membranes. Biochim Biophys Acta 135: 1–10

    Google Scholar 

  • Dylewski DP, Keenan TW (1983) Compound exocytosis of casein micelles in mammary epithelial cells. Eur J Cell Biol 31: 114–124

    Google Scholar 

  • —, Dapper CH, Valivullah HM, Deeney JT, Keenan TW (1984) Morphological and biochemical characterization of possible intracellular precursors of milk lipid globules. Eur J Cell Biol 35: 99–111

    Google Scholar 

  • —, Haralick RM, Keenan TW (1984) Three-dimensional ultrastructure of the Golgi apparatus in bovine mammary epithelial cells during lactation. J Ultrastruct Res 87: 75–85

    Google Scholar 

  • Ehrenreich JH, Bergeron JJM, Siekevitz P, Palade GE (1973) Golgi fractions prepared from rat liver homogenate. I. Isolation procedure and morphological characterization. J Cell Biol 59: 45–72

    Google Scholar 

  • Emmelot P, Bos CJ, Benedetti EL, Rûmke PH (1964) Studies on plasma membranes. I. Chemical composition and enzyme content of plasma membranes isolated from rat liver. Biochim Biophys Acta 90: 126–145

    Google Scholar 

  • Feldman JD (1961) Fine structure of the cow's udder during gestation and lactation. Lab Invest 10: 238–255

    Google Scholar 

  • Ferber E, Resch K, Wallach DFH, Imm W (1972) Isolation and characterization of lymphocyte plasma membranes. Biochim Biophys Acta 266: 494–504

    Google Scholar 

  • Finean JB, Coleman R, Mitchell RH (1984) Membranes and their cellular functions, 3rd edn. Blackwell, Oxford

    Google Scholar 

  • Fleet IR, Goode JA, Hammon MH, Laurie MS, Linzeil JL, Peaker M (1975) Secretory activity of the goat mammary glands during pregnancy and the onset of lactation. J Physiol 251: 763–773

    Google Scholar 

  • Fleisher S, Kervina M (1974) Subcellular fractionation of rat liver. Methods Enzymol 31: 6–41

    Google Scholar 

  • Franke WW, Keenan TW (1979) Interaction of secretory vesicle membrane coat structures with membrane free areas of forming milk lipid globules. J Dairy Sci 62: 1322–1325

    Google Scholar 

  • —, Deumling B, Ermen B, Jarasch E-D, Kleinig H (1970) Nuclear membranes from mammalian liver. I. Isolation procedure and general characterization. J Cell Biol 46: 379–395

    Google Scholar 

  • —, Heid HW, Grund C, Winter S, Freudenstein C, Schmid E, Jarasch E-D, Keenan TW (1981) Antibodies to the major insoluble milk fat globule membrane-associated protein: specific location in apical regions of lactating epithelial cells. J Cell Biol 89: 485–494

    Google Scholar 

  • —, Lüder MR, Kartenbeck J, Zerban H, Keenan TW (1976) Involvement of vesicle coat material in casein secretion and surface regeneration. J Cell Biol 69: 173–195

    Google Scholar 

  • Freudenstein C, Keenan TW, Eigel WN, Sasaki M, Stadier J, Franke WW (1979) Preparation and characterization of the inner coat material associated with fat globule membranes from bovine and human milk. Exp Cell Res 118: 277–294

    Google Scholar 

  • Gratzl M, Torp-Pedersen C, Dartt D, Tre M, Thorn NA (1980) Isolation and characterization of secretory vesicles from bovine neurohypophyses. Hoppe-Seylers Z Physiol Chem 361: 1615–1628

    Google Scholar 

  • Greene LJ, Hirs CHW, Palade GE (1963) On the protein composition of bovine pancreas zymogen granules. J Biol Chem 238: 2054–2070

    Google Scholar 

  • Greenwalt DE, Mather IH (1985) Characterization of an apically derived epithelial membrane glycoprotein from bovine milk, which is expressed in capillary endothelia in diverse tissues. J Cell Biol 100: 397–408

    Google Scholar 

  • Grove SN, Bracker CE, Morré DJ (1968) Cytomembrane differentiation in the endoplasmic reticulum-Golgi apparatus vesicle complex. Science 161: 171–173

    Google Scholar 

  • Hauser H, Howell K, Dawson RMC, Bowyer DE (1980) Rabbit small intestinal brush border membrane preparation and lipid composition. Biochim Biophys Acta 602: 567–577

    Google Scholar 

  • Heid HW, Winter S, Bruder G, Keenan TW, Jarasch E-D (1983) Butyrophilin, an apical plasma membrane-associated glycoprotein characteristic of lactating mammary glands of diverse species. Biochim Biophys Acta 728: 228–238

    Google Scholar 

  • Helminen HJ, Ericsson JLE (1968) Studies on mammary gland involution. I. On the ultrastructure of the lactating mammary gland. J Ultrastruct Res 25: 193–213

    Google Scholar 

  • Hokin LE (1985) Receptors and Phosphoinositide-generated second messengers. Annu Rev Biochem 54: 205–235

    Google Scholar 

  • Hollmann KH (1974) Cytology and fine structure of the mammary gland. In: Larson BL, Smith VR (eds) Lactation: a comprehensive treatise, vol 1. Academic Press, New York, pp 3–95

    Google Scholar 

  • Hood LF, Patton S (1973) Isolation and characterization of intracellular lipid droplets from bovine mammary tissue. J Dairy Sci 56: 858–863

    Google Scholar 

  • Horisberger M, Rosset J, Vonlanthen M (1977) Location of glycoproteins on milk fat globule membrane by scanning and transmission electron microscopy, using lectin-labelled gold granules. Exp Cell Res 109: 361–369

    Google Scholar 

  • House PDR, Poulis P, Weidemann MJ (1972) Isolation of a plasmamembrane subfraction from rat liver containing an insulin-sensitive cyclic-AMP phosphodiesterase. Eur J Biochem 24: 429–437

    Google Scholar 

  • Huang CM, Keenan TW (1971) Membranes of mammary gland: I. Bovine mammary mitochondria. J Dairy Sci 54: 1395–1405

    Google Scholar 

  • Huggins JW, Carraway KL (1976) Purification of plasma membranes from rat mammary gland by a density perturbation procedure. J Supramol Struct 5: 59–63

    Google Scholar 

  • —, Trenbeath TP, Chesnut RW, Carraway CAC, Carraway KL (1980) Purification of plasma membranes of rat mammary gland: compositions of subfractions with rat milk fat globule membrane. Exp Cell Res 126: 279–288

    Google Scholar 

  • Jarasch E-D, Bruder G, Keenan TW, Franke WW (1977) Redox constituents in milk fat globule membranes and rough endoplasmic reticulum from lactating mammary gland. J Cell Biol 73: 223–241

    Google Scholar 

  • —, Grund C, Bruder G, Heid HW, Keenan TW, Franke WW (1981) Localization of xanthine oxidase in mammary gland epithelium and capillary endothelium. Cell 25: 67–82

    Google Scholar 

  • Jenness R, Koops J (1962) Preparation and properties of a salt solution which simulates milk ultrafiltrate. Neth Milk Dairy J 16: 153–164

    Google Scholar 

  • Johnson VG, Mather IH (1985) Monoclonal antibodies prepared against PAS-I, butyrophilin and GP-55 from guinea-pig milkfat-globule membrane bind specifically to the apical pole of secretory-epithelial cells in lactating mammary tissue. Exp Cell Res 156: 144–158

    Google Scholar 

  • Jones DH, Rosano TG (1972) Studies of mitochondrial development prior to lactogenesis in the mouse mammary gland. Arch Biochem Biophys 153: 130–138

    Google Scholar 

  • Kamat VB, Wallach DFH (1965) Separation and partial purification of plasma-membrane fragments from Ehrlich ascites carcinoma microsomes. Science 148: 1343–1345

    Google Scholar 

  • Kanno C (1980) Recent studies on milk fat globule membrane with special reference to the constituent proteins. Jap J Zootech Sci 51: 75–88

    Google Scholar 

  • —, Kim D-H (1990) A simple procedure for the preparation of bovine milk fat globule membrane and a comparison of its composition, enzymatic activities and electrophoretic properties with those prepared by other methods. Agricult Biol Chem 54: 2845–2854

    Google Scholar 

  • —, Hattori H, Yamauchi K (1982) Isolation and characterization of plasma membrane from lactating bovine mammary gland. Biochim Biophys Acta 689: 121–134

    Google Scholar 

  • — — — (1987 a) Characterization of plasma membrane proteins from lactating bovine mammary gland. Agricult Biol Chem 51: 1325–1332

    Google Scholar 

  • — — — (1987 b) Lipid composition of plasma membranes isolated from lactating bovine mammary gland. Agricult Biol Chem 51: 2995–3001

    Google Scholar 

  • —, Ohmura Y, Yanagisawa H (1989) Comparative study of the enzymatic properties of phosphodiesterase I from the plasma membrane of lactating bovine mammary gland and bovine milk fat globule membrane. Agricult Biol Chem 53: 607–613

    Google Scholar 

  • Keenan TW (1974) Membranes of mammary gland. IX. Concentration of glycosphingolipid galactosyl and sialyltransferases in Golgi apparatus from bovine mammary gland. J Dairy Sci 57: 187–192

    Google Scholar 

  • —, Dylewski DP (1985) Aspects of intracellular transit of serum and lipid phases of milk. J Dairy Sci 68: 1025–1040

    Google Scholar 

  • —, Huang CM (1972) Membranes of mammary gland: VI. Lipid and protein composition of Golgi apparatus and rough endoplasmic reticulum from bovine mammary gland. J Dairy Sci 55: 1586–1596

    Google Scholar 

  • —, Morré DJ (1970) Phospholipid class and fatty acid composition of Golgi apparatus isolated from rat liver and comparison with other cell fraction. Biochemistry 9: 19–25

    Google Scholar 

  • —, Dylewski DP, Woodford TA, Ford RH (1983) Origin of milk fat globules and the nature of the milk fat globule membrane. In: Fox PF (ed) Developments in dairy chemistry, vol 2. Applied Scientific Publishers, London, pp 83–118

    Google Scholar 

  • —, Franke WW, Mather IH, Morré DJ (1978) Endomembrane composition and function in milk formation. In: Larson BL (ed) Lactation. A comprehensive treatise, vol 4. Academic Press, New York, pp 405–436

    Google Scholar 

  • —, Heid HW, Stadler J, Jarasch E-D, Franke WW (1982) Tight attachment of fatty acids to proteins associated with milk lipid globule membrane. Eur J Cell Biol 26: 270–276

    Google Scholar 

  • —, Huang CM, Morré DJ (1972 a) Membranes of mammary gland: III. Lipid composition of Golgi apparatus from rat mammary gland. J Dairy Sci 55: 51–57

    Google Scholar 

  • — (1972 b) Membranes of mammary gland: V. Isolation of Golgi apparauts and rough endoplasmic reticulum from bovine mammary gland. J Dairy Sci 55: 1577–1585

    Google Scholar 

  • —, Mather IH, Dylewski DP (1988) Physical equilibria: lipid phase. In: Wong NP (ed) Fundamentals of dairy chemistry, 3rd edn. Van Nostrand Reinhold, New York, pp 511–582

    Google Scholar 

  • —, Morré DJ, Cheetham RD (1970 a) Lactose synthesis by a Golgi apparatus fraction from rat mammary gland. Nature 228: 1105–1106

    Google Scholar 

  • — —, Huang CM (1974) Membranes of the mammary gland. In: Larson BL, Smith VR (eds) Lactation. A comprehensive treatise, vol 2. Academic Press, New York, pp 191–233

    Google Scholar 

  • —, Olson DE, Yunghans WN, Patton S (1970 b) Biochemical and morphological comparison of plasma membrane and milk fat globule membrane from bovine mammary gland. J Cell Biol 44: 80–93

    Google Scholar 

  • —, Olson DE, Mollenhauer HH (1971) Origin of the milk fat globule membrane. J Dairy Sci 54: 295–299

    Google Scholar 

  • —, Powell KM, Sasaki M, Eigel WN, Franke WW (1977) Membranes of mammary gland. XIV. Isolation and partial characterization of a high molecular weight glycoprotein fraction from bovine milk fat globule membrane. Cytobiologie 15: 96–115

    Google Scholar 

  • —, Sasaki M, Eigel WN, Morré DJ, Franke WW, Zulak IM, Bushway AA (1979) Characterization of a secretory vesicle-rich fraction from lactating bovine mammary gland. Exp Cell Res 124: 47–61

    Google Scholar 

  • —, Valivullah HM, Dunlevy JT (1989) Isolation of plasma membranes from mammary gland by two-phases polymer partitioning. Anal Biochem 177: 194–198

    Google Scholar 

  • Kinsella JE (1972) The lipid composition of microsomal preparations from lactating bovine mammary tissue. Lipids 7: 165–170

    Google Scholar 

  • Kitchen BJ (1974) A comparison of the properties of membranes isolated from bovine skim milk and cream. Biochim Biophys Acta 356: 257–269

    Google Scholar 

  • Kleinig H (1970) Nuclear membranes from mammalian liver. II. Lipid composition. J Cell Biol 46: 396–402

    Google Scholar 

  • Knudson CM, Stemberger BH, Patton S (1978) Effect of colchicine on ultrastructure of the lactating mammary cell: membrane involvement and stress on the Golgi apparatus. Cell Tissue Res 195: 169–181

    Google Scholar 

  • Kuhn NJ, White A (1975) The topography of lactose synthesis. Biochem J 148: 77–84

    Google Scholar 

  • — — (1977) The role of nucleoside diphosphatase in a uridine nucleotide cycle associated with lactose synthesis in rat mammarygland Golgi apparatus. Biochem J 168: 423–433

    Google Scholar 

  • —, Wooding FBP, White A (1980) Properties of galactosyltransferase-enriched vesicles of Golgi membranes from lactating-rat mammary gland. Eur J Biochem 103: 377–385

    Google Scholar 

  • Kurosumi K, Kobayashi Y, Baba N (1968) The fine structure of mammary glands of lactating rats with special reference to the apocrine secretion. Exp Cell Res 50: 177–179

    Google Scholar 

  • Lauter CJ, Solyom A, Trams EG (1972) Comparative studies on enzyme markers of liver plasma membranes. Biochim Biophys Acta 266: 511–523

    Google Scholar 

  • Linzell JL (1974) Mammary blood flow and methods of identifying and measuring precursors of milk. In: Larson BL, Smith VR (eds) Lactation. A comprehensive treatise, vol 1. Academic Press, New York, pp 143–225

    Google Scholar 

  • —, Peaker M (1971) Mechanism of milk secretion. Physiol Rev 51: 564–597

    Google Scholar 

  • Lucy JA, Ahkong QF (1986) An osmotic model for the fusion of biological membranes. FEBS Lett 199: 1–11

    Google Scholar 

  • Mather IH, Keenan TW (1975) Studies on the structure of milk fat globule membrane. J Membr Biol 21: 65–85

    Google Scholar 

  • McPherson AV, Kitchen BJ (1983) Reviews of the progress of dairy science: the bovine milk fat globule membrane-its formation, composition, structure and behaviour in milk and dairy products. J Dairy Res 50: 107–133

    Google Scholar 

  • Meldolesi J, Cova D (1972) Composition of cellular membranes in the pancreas of the guinea pig. IV. Polyacrylamide gel electrophoresis and amino acid composition of membrane proteins. J Cell Biol 55: 1–18

    Google Scholar 

  • —, Borgese N, De Camilli P, Ceccarelli B (1978) Cytoplasmic membranes and the secretory process. In: Poste G, Nicolson GL (eds) Cell surface reviews, vol 5, membrane fusion. Elsevier/North-Holland, Amsterdam, pp 509–627

    Google Scholar 

  • —, Jamieson JD, Palade GE (1971) Composition of cellular membranes in the pancreas of the guinea pig. I. Isolation of membrane fractions. J Cell Biol 49: 109–129

    Google Scholar 

  • Merrit WD, Morré DJ (1973) A glycosyl transferase of high specific activity in secretory vesicles from isolated Golgi apparatus of rat liver. Biochim Biophys Acta 304: 397–407

    Google Scholar 

  • Minasian LC, Jabara AG (1974) A technique for isolating pure, variable parenchymal cells and their nuclei from rat mammary gland. Anal Biochem 58: 395–403

    Google Scholar 

  • Mollenhauer HH, Morré DJ (1966) Golgi apparatus and plant secretion. Annu Rev Plant Physiol 17: 27–46

    Google Scholar 

  • Morré DJ (1973) Isolation and purification of organelles and endomembrane components from rat liver. In: Chrispeels MJ (ed) Molecular techniques and approaches in developmental biology. Wiley, New York, pp 1–27

    Google Scholar 

  • — (1977) The Golgi-apparatus and membrane biogenesis. In: Poste G, Nicolson GL (eds) Cell surface reviews, vol 4, the synthesis, assembly and turnover of cell surface. Elsevier/North-Holland, Amsterdam, pp 1–83

    Google Scholar 

  • —, Mollenhauer HH (1974) The endomembrane concept: a functional integration of endoplasmic reticulum and Golgi apparatus. In: Robards AW (ed) Dynamic aspects of plant ultrastructure. McGraw-Hill, New York, pp 84–137

    Google Scholar 

  • —, Kartenbeck J, Franke WW (1979) Membrane flow and interconversions among endomembranes. Biochim Biophys Acta 559: 71–152

    Google Scholar 

  • Mulder H, Walstra P (1974) The milk fat globule. Commonwealth Agricultural Bureaux, Farnham Royal, Bucks, England

    Google Scholar 

  • Nelson WL, Butow RA (1967) Guinea pig mammary gland mitochondria. Methods Enzymol 10: 103–104

    Google Scholar 

  • Neville DM (1960) The isolation of a cell membrane fraction from rat liver. J Biophys Biochem Cytol 8: 413–422

    Google Scholar 

  • —, Watters CD (1983) Secretion of calcium into milk: review. J Dairy Sci 66: 371–380

    Google Scholar 

  • Nickerson SC, Keenan TW (1979) Distribution and orientation of microtubules in milk secreting epithelial cells of rat mammary gland. Cell Tissue Res 202: 303–312

    Google Scholar 

  • —, Akers RM, Weinland BT (1982) Cytoplasmic organization and quantitation of microtubules in bovine mammary epithelial cells during lactation and involution. Cell Tissue Res 223: 421–430

    Google Scholar 

  • —, Smith JJ, Keenan TW (1980 a) Role of microtubules in milk secretion-action of colchicine on microtubules and exocytosis of secretory vesicles in rat mammary epithelial cells. Cell Tissue Res 207: 361–376

    Google Scholar 

  • — — (1980 b) Ultrastructural and biochemical response of rat mammary epithelial cells to vinblastine sulphate. Eur J Cell Biol 23: 115–121

    Google Scholar 

  • Nicolson GL (1976) Transmembrane control of the receptors on normal and tumor cells. I. Cytoplasmic influence over cell surface components. Biochim Acta 457: 57–108

    Google Scholar 

  • Nishizuka Y (1984) The role of protein kinase C in cell surface signal transduction and tumour promotion. Nature 308: 693–698

    Google Scholar 

  • Novikoff PM, Novikoff AB, Quintana N, Hauw J-J (1971) Golgi apparatus, GERL, and lysosomes of neurons in dorsal root ganglia, studied by thick section and thin section cytochemistry. J Cell Biol 50: 859–886

    Google Scholar 

  • Olliver-Bousquet M (1979) Effects de la cytochalasin B et de la colchicine sur l'action rapide de la prolactine dans la glande mammaire de lapine en lactation. Eur J Cell Biol 19: 168–174

    Google Scholar 

  • Parson JG, Patton S (1967) Two-dimensional thin-layer chromatography of polar lipids from milk and mammary tissue. J Lipid Res 8: 696–698

    Google Scholar 

  • Patton S (1970) Correlative relationship of cholesterol and sphingomyelin in cell membrane. J Theoret Biol 29: 489

    Google Scholar 

  • — (1973) Origin of milk fat globule. J Amer Oil Chem Soc 50: 178–185

    Google Scholar 

  • — (1974) Reversible suppression of lactation by colchicine. FEBS Lett 48: 85–87

    Google Scholar 

  • — (1976) Mechanism of secretion: effect of colchicine and vincristine on composition and flow of milk in the goat. J Dairy Sci 59: 1414–1419

    Google Scholar 

  • — (1978) Milk secretion of the cellular level: a unique approach to the mechanism of exocytosis. J Dairy Sci 61: 643–650

    Google Scholar 

  • —, Fowkes FM (1967) The role of the plasma membrane in the secretion of milk fat. J Theoret Biol 48: 85–87

    Google Scholar 

  • —, Huston GE (1987) Differences between individuals in high-Mr glycoproteins from human mammary epithelia. FEBS Lett 216: 151–154

    Google Scholar 

  • —, Jensen RG (1976) Biomédical aspects of lactation. Pergamon Press, New York

    Google Scholar 

  • —, Keenan TW (1971) The relationship of milk phospholipids to membranes of the secretory cell. Lipids 6: 58–61

    Google Scholar 

  • — — (1975) The milk fat globule membrane. Biochim Biophys Acta 415: 273–309

    Google Scholar 

  • —, Trams EG (1971) The presence of plasma membrane enzymes on the surface of bovine milk fat globules. FEBS Lett 14: 230–232

    Google Scholar 

  • —, Durdan A, McCarthy RD (1964) Structure and synthesis of milk fat. VI. Unity of the phospholipids in milk. J Dairy Sci 47: 489–495

    Google Scholar 

  • —, Hood LF, Patton JS (1969) Negligible release of cardiolipin during milk secretion by the ruminant. J Lipid Res 10: 260–266

    Google Scholar 

  • —, Huston GE, Jenness R, Vaucher Y (1989) Differences between individuals in high molecular weight glycoproteins from mammary epithelia of several species. Biochim Biophys Acta 980: 333–338

    Google Scholar 

  • —, McCarthy RD, Plantz PE, Lee RF (1973) Phosphohpid incorporation into plasma membrane of lactating mammary cell with special reference to sphingomyelin. Nature New Biol 241: 241–242

    Google Scholar 

  • —, Stemberger BH, Knudson CM (1977) The suppression of milk fat globule secretion by colchicine: an effect coupled to inhibition of exocytosis. Biochim Biophys Acta 499: 404–410

    Google Scholar 

  • Peixoto de Menezes A, Pinto da Silva P (1978) Freeze-fracture observations of the lactating rat mammary gland: membrane events during milk fat secretion. J Cell Biol 76: 767–778

    Google Scholar 

  • Pinto da Silva P, Peixoto de Menezes A, Mather IH (1980) Structure and dynamics of the bovine milk fat globule membrane viewed by freeze fracture. Exp Cell Res 125: 127–139

    Google Scholar 

  • Pitelka DR, Hamamoto ST (1977) Form and function in mammary epithelium: the interpretation of ultrastructure. J Dairy Sci 60: 643–654

    Google Scholar 

  • Plantz PE, Patton S (1973) Plasma membrane fragments in bovine and caprine skim milks. Biochim Biophys Acta 291: 51–60

    Google Scholar 

  • — —, Keenan TW (1973) Further evidence of plasma membrane material in skim milk. J Dairy Sci 56: 978–983

    Google Scholar 

  • Pocius PA, Dreels JM, Devery-Pocius JE, Baumrucker CR (1984) Techniques for preparation of bovine mammary smooth membranes. J Dairy Sci 67: 2055–2061

    Google Scholar 

  • Ray TK, Skipski VP, Barclay M, Essner E, Archibald FM (1969) Lipid composition of rat liver plasma membranes. J Biol Chem 244: 5528–5536

    Google Scholar 

  • Rosano TG, Jones DH (1976) Developmental changes in mitochondria during the transition into lactation in the mouse mammary gland. I. Behavior on isopycnic gradient centrifugation. J Cell Biol 69: 573–580

    Google Scholar 

  • Rosano TG, Lee SK, Jones DH (1976) Developmental changes in mitochondria during the transition into lactation in the mouse mammary gland. II. Membrane marker enzymes and membrane ultrastructure. J Cell Biol 69: 581–588

    Google Scholar 

  • Rosenberg SA, Guidotti G (1968) The protein of human erythrocyte membranes. I. Preparation, solubilization, and partial characterization. J Biol Chem 243: 1985–1992

    Google Scholar 

  • Saacke RG, Heald CW (1974) Cytological aspects of milk formation and secretion. In: Larson BL, Smith VR (eds) Lactation. A comprehensive treatise, vol 2. Academic Press, New York, pp 147–189

    Google Scholar 

  • Sasaki M, Keenan TW (1978) Membranes of mammary gland. XV. 5-Thioglucose decrease lactose content and inhibits secretory vesicle maturation in lactating rat mammary gland. Exp Cell Res 111: 413–425

    Google Scholar 

  • —, Eigel WN, Keenan TW (1978) Lactose and major milk proteins are present in secretory vesicle-rich fractions from lactating mammary gland. Proc Natl Acad Sci USA 75: 5020–5024

    Google Scholar 

  • Sekhi KK, Pitelka DR, De Ome KB (1967) Studies of mouse mammary glands. I. Cytomorphology of the normal mammary gland. J Natl Cancer Inst 39: 459–490

    Google Scholar 

  • Sharma A, Dahiya R (1988) The lipid composition of plasma membrane from goat mammary gland. Biochem Cell Biol 66: 1355–1359

    Google Scholar 

  • —, Ray TK (1982) Isolation of lactating goat mammary plasma membranes. Indian J Exp Biol 20: 257–259

    Google Scholar 

  • Shimizu M, Yamauchi K (1982) Isolation and characterization of mucin-like glycoprotein in human milk fat globule membrane. J Biochem 91: 515–524

    Google Scholar 

  • — —, Miyauchi Y, Sakurai T, Tokugawa K, Mcllhinney AJ (1986) High-Mr glycoprotein profiles in human milk serum and fatglobule membrane. Biochem J 233: 725–730

    Google Scholar 

  • Shin BC, Ebner KE, Hudson BG, Carraway KL (1975) Membrane glycoprotein difference between normal lactating mammary tissue and the R3230 AC mammary tumor. Cancer Res 35: 1135–1140

    Google Scholar 

  • Siekevitz P (1975) Dynamics of intracellular membranes. In: Weissmann G, Claiborne R (eds) Cell membranes. Biochemistry, cell biology and pathology. HP, New York, pp 115–122

    Google Scholar 

  • Silcock WR, Patton S (1972) Correlative secretion of protein, lactose and K+ in milk of the goat. J Cell Physiol 79: 151–154

    Google Scholar 

  • Singer SJ, Nicholson GL (1972) The fluid mosaic model of the structure of cell membranes. Science 175: 720–731

    Google Scholar 

  • Smith AD, Winkler H (1967) A simple method for the isolation of adrenal chromaffin granules on a large scale. Biochem J 103: 480–482

    Google Scholar 

  • Sokka TK, Patton S (1983) In vivo effects of colchicine on milk fat lobule membrane. Biochim Biophys Acta 731: 1–8

    Google Scholar 

  • Soulier S, Gaye P (1981) EnzymaticO-glycosylation of k-caseinomacropeptide by ovine mammary Golgi membranes. Biochimie 63: 619–628

    Google Scholar 

  • Stemberger BH, Patton S (1981) Relationships of size, intracellular location, and time required for secretion of milk fat droplets. J Dairy Sci 64: 422–426

    Google Scholar 

  • —, Walsh RM, Patton S (1984) Morphometric evaluation of lipid droplet assocaitions with secretory vesicles, mitochondria and other components in the lactating cell. Cell Tissue Res 236: 471–475

    Google Scholar 

  • Stewart PS, Puppione DL, Patton S (1972) The presence of microvilli and other membrane fragments in the non-fat phase of bovine milk. Z Zellforsch 123: 161–167

    Google Scholar 

  • Takeuchi M, Terayama H (1965) Preparation and chemical composition of rat liver cell membranes. Exp Cell Res 40: 32–44

    Google Scholar 

  • Thines-Sempoux D, Amar-Costesec A, Beaufay H, Berthet J (1969) The association of cholesterol, 5′-nucleotidase, and alkaline phosphodiesterase I with a distinct group of microsomal particles. J Cell Biol 43: 189–192

    Google Scholar 

  • Touster O, Aronson NN Jr, Dulaney JT, Hendrickson H (1970) Isolation of rat liver plasma membranes. Use of nucleotide pyrophosphatase and phosphodiesterase I as marker enzymes. J Cell Biol 47: 604–618

    Google Scholar 

  • Tsai C-M, Chen K-Y, Canellakis ES (1975) Isolation and characterization of the plasma membrane of L-1210 cells. lodination as a marker for the plasma membrane. Biochim Biophys Acta 401: 196–212

    Google Scholar 

  • Van Hoeven RP, Emmelot P (1972) Studies on plasma membranes. XVIII. Lipid class composition of plasma membranes isolated from rat and mouse liver and hepatoma. J Membrane Biol 9: 105–126

    Google Scholar 

  • Wallach DFH, Kamat VB (1964) Plasma and cytoplasmic membrane fragments from Ehrlich ascites carcinoma. Proc Natl Acad Sci USA 52: 721–728

    Google Scholar 

  • —, Lin PS (1973) A critical evaluation of plasma membrane fractionation. Biochim Biophys Acta 300: 211–254

    Google Scholar 

  • Walstra P (1969) Studies on milk fat dispersion. II. The globule-size distribution of cow's milk. Netherl Milk Dairy J 23: 99–110

    Google Scholar 

  • —, Jenness R (1984) Dairy chemistry and physics. Wiley, New York

    Google Scholar 

  • Warren K (1975) Isolation and properties of natural membranes. In: Weissmann G, Claiborne R (eds) Cell membranes. Biochemistry, cell biology and pathology, HP, New York, pp 65–73

    Google Scholar 

  • Wellings SR (1969) Ultrastructural basis of lactogenesis. In: Reynolds M, Folley SJ (eds) Lactogenesis. University of Pennsylvania Press, Philadelphia, pp 5–25

    Google Scholar 

  • Welsch U, Singh S, Buchheim W, Patton S (1984) Internalization of ferritin-concanavalin A by the lactating mammary cell in vivo. Cell Tissue Res 235: 433–438

    Google Scholar 

  • —, Buchheim W, Schmacher U, Schinko I, Patton S (1988) Structural, histochemical and biochemical observations on horse milkfat-globule membranes and casein micelles. Histochemistry 88: 357–365

    Google Scholar 

  • Whaley WG (1975) The Golgi apparatus. Springer, Wien New York [Alfert M et al (eds) Cell biology monographs, vol 2]

    Google Scholar 

  • Wibo M, Godelaine D, Amar-Costesec A, Beaufay H (1976) Subcellular location of glycosyltransferase in rat liver. In: Preisig R, Bircher J, Paumgartner G (eds) The liver. Editio Cantor, Aulendorff, pp 70–83

    Google Scholar 

  • Wooding FBP (1971 a) The mechanism of secretion of the milk fat globule. J Cell Sci 9: 805–821

    Google Scholar 

  • — (1971 b) The structure of the milk fat globule membrane. J Ultrastruct Res 37: 288–400

    Google Scholar 

  • — (1973) Formation of the milk fat globule membrane without participation of the plasmalemma. J Cell Sci 13: 221–235

    Google Scholar 

  • — (1974) Milk fat globule membrane material in skim milk. J Dairy Res 41: 331–337

    Google Scholar 

  • — (1977) Comparative mammary fine structure. In: Peaker M (ed) Comparative aspects of lactation. Academic Press, London, pp 1–41

    Google Scholar 

  • —, Kemp P (1975) Ultrastructure of the milk fat globule membrane with and without triglyceride. Cell Tissue Res 165: 113–127

    Google Scholar 

  • —, Morgan G (1978) Calcium localization in lactating rabbit mammary secretory cells. J Ultrastruct Res 63: 323–333

    Google Scholar 

  • —, Peaker M, Linzeil JL (1970) Theories of milk secretion: evidence from the electron microscopic examination of milk. Nature 226: 762–764

    Google Scholar 

  • Zilversmit DB (1984) Lipid transfer proteins. J Lipid Res 25: 1563–1569

    Google Scholar 

  • Zulak IM, Keenan TW (1983) Citrate accumulation by a Golgi apparatus-rich fraction from lactating bovine mammary gland. Int J Biochem 15: 747–750

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Dedicated to Professor Stuart Patton on the occasion of his 70th birthday.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kanno, C. Secretory membranes of the lactating mammary gland. Protoplasma 159, 184–208 (1990). https://doi.org/10.1007/BF01322601

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01322601

Keywords

Navigation