Summary
It is generally accepted that variations in membrane cholesterol content affect the fluidity of the bilayer, thus altering its permeability. In the biological membranes, in physiological conditions, a high cholesterol content rigidifies the bilayer decreasing its permeability, a lower cholesterol content induces the opposite effect by increasing the permeability. Since differences in the epithelial permeability for short chain fatty acids have previously been demonstrated in the proximal and distal colon of the guinea pig, these two regions were investigated to establish whether differences in membrane cholesterol content of the absorbing cells can be demonstrated. Freeze-fracture replicas of filipin-treated colonic tissue were used. The results show that in the proximal colon the density of filipin cholesterol complexes located on the luminal plasma membrane of the columnar absorbing cells was significantly higher (about twice) than in the distal colon. Therefore the lower amount of cholesterol present in the membrane of the absorbing cells in the distal colon indicates a greater fluidity of the membranes of the epithelial cells in this region. Such fluidity could be correlated to the higher absorption rates of shortchain fatty acids characteristic of this region.
Similar content being viewed by others
References
Brasitus TA, Schachter D (1982) Cholesterol biosynthesis and modulation of membrane cholesterol and lipid dynamics in rat intestinal microvillus membranes. Biochemistry 21:2241–2246
Brasitus TA, Dudeja PK, Worman HJ, Foster ES (1986) The lipid fluidity of rat colonic brush-border membrane vesicles modulates Na+ H+ exchange and osmotic water permeability. Biochim Biophys Acta 855:16–24
Brasitus TA, Dudeja PK, Dahiya R, Brown MD (1987) 1,2-Dimethylhydrazine-induced alterations in colonic plasma membrane fluidity: restriction to the luminal region. Biochim Biophys Acta 896:311–317
Brasitus TA, Dudeja PK, Foster ES (1988) 1,2-Dimethylhydrazine-induced alterations in Na+ — H+ exchange in rat colonic brushborder membrane vesicles. Biochim Biophys Acta 938:483–488
Bullivant S (1981) Possible relationships between tight junction structure and function. In: Macknight ADC, Leader JP (eds) Epithelial ion and water transport. Raven, New York, pp 265–275
Chapman D (1983) Biomembrane fluidity: the concept and its development. In: Aloia RC (ed) Membrane fluidity in biology, vol 2. Academic Press, New York, pp 1–42
Chapman D, Byrne P, Shipley GG (1966) The physical properties of phospholipids. I. Solid state and mesomorphic properties of some 2,3-diacyl-DL-phosphatidylethanolamines. Proc R Soc (Serie A) 290:115–142
Cooper RA, Strauss JF (1984) Regulation of cell membrane cholesterol. In: Shinitzky M (ed) Physiology of membrane fluidity, vol 1. CRC Press, Boca Raton, pp 73–97
De Kruijff B, Demel RA (1974) Polyene antibiotic-sterol interactions in membranes of Acholeplasma laidlawii cells and lecithin liposomes. III. Molecular structure of the polyene antibiotic-cholesterol complexes. Biochim Biophys Acta 339:57–70
De Kruijff B, Gerritsen WJ, Oerlemans A, van Dijck PWM, Demel RA, van Deenen LLM (1974) Polyene antibiotic-sterol interactions in membranes of Acholeplasma laidlawii cells and lecithin liposomes. II. Temperature dependence of the polyene antibiotic-sterol complex formation. Biochim Biophys Acta 339:44–56
Dudeja PK, Foster ES, Dahiya R, Brasitus TA (1987a) Modulation of Na+-H+ exchange by ethinyl estradiol in rat colonic brush-border membrane vesicles. Biochim Biophys Acta 899:222–228
Dudeja PK, Foster ES, Brasitus TA (1987b) Modulation of rat distal colonic brush-border membrane Na+-H+ exchange by dexamethasone: role of lipid fluidity. Biochim Biophys Acta 905:485–493
Engelhardt W v, Rechkemmer G (1983) Absorption of inorganic ions and short-chain fatty acids in the colon of mammals. In: Gilles-Baillien M, Gilles R (eds) Intestinal transport. Springer, Berlin Heidelberg New York, pp 26–45
Jain MK (1975) Role of cholesterol in biomembranes and related systems. Curr Top Membr Transp 6:1–57
Karnovsky MJ (1982) Intramembranous cytochemistry: a perspective. Lab Invest 46:637–639
Kottra G, Frömter E (1983) Functional properties of the paracellular pathway in some leaky epithelia. J Exp Biol 106:217–229
Lee AG (1983) Lipid phase transitions and mixtures. In: Aloia RC (ed) Membrane fluidity in biology, vol 2. Academic Press, New York, pp 84–89
Le Grimellec Ch, Carrière S, Cardinal J, Giocondi M-C (1983) Fluidity of brush border and basolateral membranes from huan kidney cortex. Am J Physiol 245:F227-F231
Lippert JL, Peticolas WL (1971) Laser Raman investigation of the effect of cholesterol on conformational changes in dipalmitoyl lecithin multilayers. Proc Natl Acad Sci USA 68:1572–1576
Luciano L, Reale E, Rechkemmer G, Engelhardt W v (1984) Structure of zonulae occludentes and the permeability of the epithelium to short-chain fatty acids in the proximal and the distal colon of guinea pig. J Membr Biol 82:145–156
Luciano L, Engelhardt W v, Rönnau K, Reale E (1987) Different distribution of filipin-cholesterol complexes (FCC) in the proximal and distal colonic epithelium of guinea pig. Eur J Cell Biol, suppl 19 (vol 44):36
Norman AW, Demel RA, De Kruijff B, van Deenen LLM (1972) Studies on the biological properties of polyene antibiotics. Evidence for the direct interaction of filipin with cholesterol. J Biol Chem 247:1918–1929
Orci L, Montesano R, Meda P, Malaisse-Lagae F, Brown D, Perrelet A, Vassalli P (1981) Heterogeneous distribution of filipinholesterol complexes across the cisternae of the Golgi apparatus. Proc Natl Acad Sci USA 78:293–297
Presti FT (1985) The role of cholesterol in regulating membrane fluidity. In: Aloia RC, Boggs JM (eds) Membrane fluidity in biology, vol 4. Academic Press, Orlando, pp 97–146
Robinson JM, Karnovsky MJ (1980) Evaluation of the polyene antibiotic filipin as a cytochemical probe for membrane choleserol. J Histochem Cytochem 28:161–168
Rönnau K, Guth D, Engelhardt W v (1989) Absorption of dissociated and undissociated short chain fatty acids across the colonic epithelium of guinea pig. Quart J Exp Physiol 74:511–519
Severs NJ, Robenek H (1983) Detection of microdomains in biomembranes. An appraisal of recent developments in freeze-fracture cytochemistry. Biochim Biophys Acta 737:373–408
Weibel ER (1979) Stereological methods. Vol 1 Practical methods for biological morphometry. Academic Press, London
Yeagle PL (1985) Cholesterol and the cell membrane. Biochim Biophys Acta 822:267–287
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Luciano, L., Konitz, H. & Reale, E. Localization of cholesterol in the colonic epithelium of the guinea pig: regional differences and functional implications. Cell Tissue Res. 258, 339–347 (1989). https://doi.org/10.1007/BF00239454
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00239454