Abstract
Human placental syncytiotrophoblast basal membrane plays an important role in transfer of nutrients from the mother to the growing fetus all throughout gestation. The membrane lipid composition together with the bilayer fluidity is found to be the major index in modulation of these transport processes. In the present study, the effects of changing lipid composition on the placental basal membrane fluidity and the modulating influence of the latter on membrane enzyme and transport functions with progress of gestation,were investigated. Steady-state fluorescence analysis using 1,6-diphenyl-1,3,5 hexatriene as the probe, indicated a decrease in fluorescence anisotropy of both labeled native membrane vesicles and liposomes prepared from lipids extracted from the basal membrane vesicles, signifying increased bilayer fluidity with progress of gestation. This in turn, was successfully correlated to the lowering of cholesterol content and enhanced phospholipid concentration with a steady decrease in cholesterol/phospholipid ratio during placental development. Enhanced Na+-K+-ATPase activity and steady-state glucose uptake across basal membrane with gestational progress suggested modulation of membrane protein functions by the fluidity, which was further corroborated by the increased bilayer fluidity and enzyme activity in benzyl alcohol treated basal membrane in each gestational age group.
Similar content being viewed by others
References
Williams JW, Cunningham FG, MacDonald PC, Gant NF: The placenta and fetal membranes: In Williams Obstetrics (18th ed), Appleton and Lange, Norwalk, Connecticut, 1989, p 39
Sideri M, de Virgilis G, Rainoldi R, Remotti G: The ultrastructural basis of the nutritional transfer: Evidence of different patterns in the plasma membranes of the multilayered placental barrier. Trophoblast Res 1: 15-26, 1983
Singer SJ, Nicolson GL: The fluid mosaic model of the structure of cell membranes. Science 175: 720-731, 1972
Labelle EF: Effect of cholesterol on the Valinomycin-mediated uptake of rubidium into erythrocytes and phospholipid vesicles. Biochim Biophys Acta 555: 259-269, 1979
Papahadjopoulos D, Cowden M, Kimelberg H: Role of cholesterol in membranes, effects on phospholipid-protein interactions, membrane permeability and enzymatic activity. Biochim Biophys Acta 330: 8-26, 1973
Shinitzky M, Inbar M: Microviscosity parameters and protein mobility in biological membranes. Biochim Biophys Acta 433: 133-149, 1976
Brasitus TA, Dudeja PK: Regional differences in the lipid composition and fluidity of rat colonic brush-border membranes. Biochim Biophys Acta 819: 10-17, 1985
Verkman AS, Ives HE: Water permeability and fluidity of renal basolateral membrane. Am J Physiol 250: F633-F643, 1986
Illsley NP, Lin HY, Verkman AS: Lipid structure correlated with membrane protein function in placental microvillous vesicles. Biochemistry 26: 446-454, 1987
Dipple I, Houslay MD: The activity of glucagon-stimulated adenylate cyclase from rat liver plasma membranes is modulated by the fluidity of its lipid environment. Biochem J 174: 179-190, 1978
Ghosh PK, Das T, Sa G, Mukherjea M: Gestational variation in the fluidity of human placental brush-border membrane assessed by a liposomal transfer study. Med Sci Res 20: 705-706, 1992
Ghosh PK, Mukherjea M: Increase in fluidity of human placental syncytiotrophoblastic brush-border membrane with advancement of gestational age: A fluorescence polarisation study. Biochim Biophys Acta 1236: 317-323, 1995
Chaudhuri D, Kushari J, Mukherjea M: Occurrence of phosphodiesterase-IV in the developing human brain, liver and placenta. Eur J Obs Gyn Reprod Biol 13: 309-316, 1982
Illsley NP, Wang ZQ, Gray A, Sellers MC, Jacobs MM: Simultaneous preparation of paired, syncytial, microvillous and basal membranes from human placenta. Biochim Biophys Acta 1029: 218-226, 1990
Colas B, Maroux S: Simultaneous isolation of brush-border and basolateral membrane from rabbit enterocytes. Presence of brush-border hydrolases in basolateral membrane of rabbit enterocytes. Biochim Biophys Acta 600: 406-420, 1980
Shirazi SP, Beechey RB, Butterworth PJ: The use of potent inhibitors of alkaline phosphatase to investigate the role of the enzyme in intestinal transport of inorganic phosphate. Biochem J 194: 803-809, 1981
Veeger C, Der Vartarian DV, Zeylemaker WP: In: Methods in Enzymology XIII. Academic Press, New York, 1969, p 81
Dallner G, Siekevitz P, Palade GE: Biogenesis of reticulum membranes-II. Synthesis of constitutive microsomal enzymes in developing rat hepatocyte. J Cell Biol 30: 97-117, 1966
Folch J, Lees M, Sloane-Stanley GH: A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226: 497-509, 1957
Sperry WM, Brand FC: The colorimetric determination of cholesterol J Biol Chem 150: 315-324, 1943
Fiske CH, Subbarow Y: The colorimetric determination of phosphorus J Biol Chem 66: 375-400, 1925
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ: Protein measurement with folin-phenol reagent. J Biol Chem 193: 265-275, 1951
Ohyashiki T, Sakata N, Matsui K: Decrease of lipid fluidity of the porcine intestinal brush-border membranes by treatment with Malondialdehyde. J Biochem 111: 419-423, 1992
North P, Fleischer S: Alteration of synaptic membrane cholesterol/phospholipid ratio using a lipid transfer protein. J Biol Chem 258: 1242-1253, 1983
Shinitzky M, Barenholz Y: Dynamics of the hydrocarbon layer in liposomes of Lecithin and Sphingomyelin containing Diacetylphosphate. J Biol Chem 249: 2652-2657, 1974
Bissonnette JM, Black JA, Wickham WK, Acott KM: Glucose uptake into plasma membrane vesicles from the maternal surface of human placenta. J Membr Biol 58: 75-80, 1981
Pearson ES, Hartley HO: In Biometika Tables for Statisticians. Vol 1. The Syndicate of the Cambridge University Press, Cambridge, 1970, p 146
Brasitus TA, Schachter D: Lipid composition and fluidity of rat enterocyte basolateral membranes regional differences. Biochim Biophys Acta 774: 138-146, 1984
Gordon LM, Sauerheber RD, Esgate JA, Dipple I, Marchmont RJ, Houslay MD: The increase in bilayer fluidity of rat liver plasma membranes achieved by the local anaesthetic benzyl alcohol affects the activity of intrinsic membrane enzymes. J Biol Chem 255: 4519-4527, 1980
Shinitzky M, Inbar M: Difference in microviscosity induced by different cholesterol levels in the surface membrane lipid layer of normal lymphocytes and malignant lymphoma cells. J Mol Biol 85: 603-615, 1974
Shinitzky M, Barenholz Y: Fluidity parameters of rigid region determined by fluorescence polarisation. Biochim Biophys Acta 515: 367-394, 1978
Cogan U, Shinitzky M, Weber G, Nishida T: Microviscosity and order in the hydrocarbon region of phospholipid and phospholipidcholesterol dispersions determined with fluorescent probes. Biochemistry 12: 521-528, 1973
Bloch K: In: D.E. Vance and J.E. Vance (eds.) Biochemistry of Lipids and Membranes. The Benjamin/Cummings Publishing Company, California, 1985, pp 1-24
Johnson LW, Smith CH: Monosaccharide transport across microvillous membrane of human placenta. Am J Physiol 238: C160-C168, 1980
Moriss FH Jr, Boyd RDH: Placental transport. In: E. Knobil and J.D. Neill (eds). The Physiology of Reproduction. Raven, New York, 1988, pp2043-2083
Johnson LW, Smith CH: Glucose transport across the basal plasma membrane of human placental syncytiotrophoblast. Biochim Biophys Acta 815: 44-50, 1985
Smith CH, Moe AJ: Nutrient transport pathways across the epithelium of the placenta. Ann Rev Nutr 12: 183-206, 1992
Fernandez YJ, Boigegrain RM, Cambon-Gros CD, Mitjavila SE: Sensitivity of Na+-coupled D-Glucose uptake, Mg+-ATPase and sucrase to perturbations of the fluidity of brush-border membrane vesicles induced by n-aliphatic alcohols. Biochim Biophys Acta 770: 171-177, 1984
Davis RA, Kern F, Showalter R, Sutherland E, Sinensky M, Simon FR: Alterations of hepatic Na+-K+-ATPase and bile flow by estrogen: Effects on liver surface membrane lipid structure and function. Proc Natl Acad Sci USA 75: 4130-4134, 1978
Yeagle PL: Cholesterol modulation of (Na+ + K+)-APTase, ATP hydrolysing activity in the human erythrocyte. Biochim Biophys Acta 727: 39-44, 1983
Kelley LK, Smith CH, King BF: Isolation and partial characterisation of the basal cell membrane of human placental trophoblast. Biochim Biophys Acta 734: 91-98, 1983
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Sen, A., Ghosh, P.K. & Mukherjea, M. Changes in lipid composition and fluidity of human placental basal membrane and modulation of bilayer protein functions with progress of gestation. Mol Cell Biochem 187, 183–190 (1998). https://doi.org/10.1023/A:1006839711587
Issue Date:
DOI: https://doi.org/10.1023/A:1006839711587