PORE-LIKE STRUCTURES IN BIOLOGICAL MEMBRANES
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1 J. Cell Sci. 25, (1977) 157 Printed in Great Britain PORE-LIKE STRUCTURES IN BIOLOGICAL MEMBRANES L. ORCI, A. PERRELET, FRANCINE MALAISSE-LAGAE AND P. VASSALLI* Institute of Histology and Embryology, and *Department of Pathology, University of Geneva Medical School, Geneva, Switzerland SUMMARY In frccze-fracture replicas, biological membranes appear as smooth surfaces interrupted by random globular protrusions, the intramembrane particles. Smooth areas correspond to the membrane phospholipidic domain, while intramembrane particles are the morphological counterpart of membrane proteins. In the present work, examination of membranes in a variety of cell types reveals that a number of intramembrane particles contain an electron-dense spot. The spot is thought to correspond to a minute pit in the particle, filled by the platinum used in the freeze-fracture procedure. Similar images, described previously in intramembrane particles forming the specific array of the gap junction, were interpreted as hydrophilic channels bridging the interior and the exterior of the plasma membrane. Comparison between the gap junction particles and the non-junctional particles containing a dense spot suggests that these latter may too contain hydrophilic channels. The channels in random intramembrane particles would represent the morphological counterparts of the water-filled pores described in models of membrane permeability. INTRODUCTION The concept of pores in biological membranes was postulated to explain the diffusion of hydrophilic molecules across the membrane's lipid bilayer (Solomon, 1968; Woodbury, 1965). However, in spite of the fact that models of diffusion across biological membranes imply the presence of numerous pores, their morphological counterparts are lacking. The only exception described so far concerns the gap junction or nexus. This specialized area of the cell membrane represents an ionic and metabolic communication pathway between the cytoplasm of two adjacent cells (McNutt & Weinstein, 1973; Payton, Bennett & Pappas, 1969) and appears morphologically as an aggregate of subunits bridging the plasma membranes (Kreutziger, 1968; McNutt & Weinstein, 1970, 1973). Thin-section (Revel & Karnovsky, 1967) and freeze-fracture (McNutt & Weinstein, 1970) electron microscopy have shown that the subunits contain minute circular densities which were interpreted as portions of hydrophilic channels piercing the centre of each subunit (McNutt & Weinstein, 1970, 1973). In freeze-fracture, gap junction subunits appear as regularly sized and closely packed intramembrane particles on the cytoplasmic leaflet of the membrane. As reported in the present paper, a re-examination of fracture faces in a wide variety of plasma membranes indicates that a sizable number of non-junctional intramembrane particles show densities at their top. Each density would represent the filling of a hole or channel in the non-junctional particles. II CEL 25
2 158 L. Orci, A. Perrelet, F. Malaisse-Lagae and P. Vassalli MATERIALS AND METHODS Pieces of liver, adrenal, endocrine pancreas and bladder of laboratory animals (mostly rodents) were used, as well as pellets of isolated mouse myeloma cells (MOPC 315), rabbit erythrocytes and mastocytes. Samples were fixed in phosphate-buffered glutaraldehyde for various periods of time, soaked for h in 30 % phosphate-buffered glycerol and frozen in Freon 22 cooled with liquid nitrogen. Frozen tissue was freeze-fractured according to Moor & Miihlethaler (1963). Platinum-carbon replicas were observed in a Philips EM 300 electronmicroscope operating at 80 kv with initial magnifications between and times. RESULTS As indicated in Materials and methods, samples of freeze-fractured membranes are derived from a wide variety of cells and tissues. Since the general morphology of membrane fracture faces is not - at least with the available material - cell- or tissuespecific, the following description applies to all material examined. As amply documented in previous studies, the freeze-fracture appearance of biological membranes is that of smooth surfaces interrupted at random by globular protrusions, the intramembrane particles (Branton, 1969, 1971)- The smooth areas correspond to the membrane phospholipidic domain, while the particles have been shown to correspond to membrane proteins (Singer, 1974; Singer & Nicolson, 1972; Vail, Papahadjopoulos & Moscarello, 1974). During freeze-fracturing, the membrane is split in 2 halves along the middle of the phospholipid bilayer, so that each leaflet of the membrane yields the above-described picture. By convention, the freeze-fractured inner leaflet of the membrane is called the P-face, while the freeze-fractured outer leaflet is called the E-face (Branton et al. 1975). A prerequisite for the study of the fine structure of particles is the use of suitably high magnification. An initial magnification in the electron microscope of x 40000, which can be further enlarged photographically by 3-5 times, is adequate in most cases. In such conditions, examination of fracture faces of both plasma and/or intracellular membranes of all cell types studied in the present work revealed that certain intramembrane particles had a tiny black spot at their top (Fig. 1 A-K). The particles showing a black spot were not otherwise different from the remaining intramembrane particles, as far as their size and shape were concerned. The relative frequency of the spotted particles in P-fracture faces could be estimated roughly to be % of all intramembrane particles present in this face (data pooled from all the membrane types examined). No attempt was performed at a quantitative correlation between a given membrane type and its content of spotted particles. The size of the dense spot on the particles was found to vary from approximately 2 to 6 nm. The position of the dense spot on the particles seemed also subject to variation. Some dense spots appeared not to be situated at the top of the particle, but were placed sideways. In plasma membranes carrying gap junctions (Fig. 1 K) we could confirm the previous finding of McNutt & Weinstein (1970) that many of the gap junction particles do show a small density at their top. As noted by these authors, random particles with a dense spot could be observed outside the junctional area as well (see Fig. IK).
3 Pore-like structures in membranes Fig. 1. Examples of membrane fracture faces (P- or E-faces) showing intramembrane particles with pits. A pit is represented by a small dense spot present at the top of the particle; some of the pits are outlined by white circles. Since all figures were arranged with the source of platinum evaporation at the lower part of the picture (shadows, in white, are upwards), one sees that pits have various orientations with respect to the membrane plane. In all figures, the bar represents 20 nm. A, Mouse myeloma cell: plasma membrane (P-face). x B, Mouse myeloma cell: plasma membrane (Eface). x c, Rabbit mastocyte: plasma membrane (P-face). x D, Toad bladder cell: plasma membrane (P-face). x E, Endothelial cell from the rat adrenal gland: plasma membrane (P-face). x F, Rat liver (hepatocyte): membrane from the endoplasmic reticulum (P-face). x G, Rabbit erythrocyte: plasma membrane (P-face). x H, Fish islet cell: plasma membrane (P-face). x , Rat islet cell: membrane from a secretory granule (P-face). x j, Rat islet cell: plasma membrane (E-face). x K, Plasma membrane from a pancreatic islet cell (P-face). This area of the membrane contains an aggregate of closely packed intramembrane particles (gap junction) as well as randomly scattered particles. Several aggregated and dispersed particles show distinct pits at their top. X
4 160 L. Orci, A. Perrelet, F. Malaisse-Lagae and P. Vassalli DISCUSSION The observations reported above suggest the existence, in freeze-fractured membranes, of a distinct population of intramembrane particles characterized by the presence of a dense spot at their top. Given the conditions of oblique platinum shadowing necessary to obtain a freeze-fracture replica (Moor & Muhlethaler, 1963), electron-dense areas on positive prints invariably indicate an accumulation of platinum. Practically, in the case of a single direction of platinum shadowing, an accumulation of this metal will occur'either on objects raised above the fracture plane (at their side facing the source), or at the bottom of pits or cavities extending below the fracture plane. Distinction between raised objects and cavities is usually easy, since the former project a shadow while the latter do not. According to this reasoning, the dense spots situated on the top of intramembrane particles (these latter are raised structures projecting shadows) represent most likely minute pits filled by platinum. In view of the similarity of appearance between the pitted particles and gap junction subunits, it is tempting to suggest that the former may contain hydrophilic channels (pores) as well. If this is true, one might ask whether the random particles with pits do not simply represent free-floating gap junction particles, given the fluidity of the membrane (Singer, 1974; Singer & Nicolson, 1972) and the fact that gap junctions are submitted to assembly and disassembly (Decker & Friend, 1974), which may occur through aggregation or disaggregation of preformed subunits (particles). Although this possibility cannot be excluded at present, the fact that pitted particles are present in red blood cells, mastocytes, myeloma cells and leucocytes as well as in sperm cells (Friend & Fawcett, 1974), all of which are free cells which do not share gap junctions, renders it less likely. In summary, the data indicate (a) that the presence of densities at the top of intramembrane particles is in favour of the presence of channels (pores) in these particles; and (b) that the channels may represent the pores assumed to account for the diffusion of hydrophilic molecules across biological membranes. This work was supported by grants no s and from the Swiss National Science Foundation. REFERENCES BRANTON, D. (1969). Membrane structure. A. Rev. PL Physiol. 20, BRANTON, D. (1971). Freeze-etching studies of membrane structure. Phil. Trans. R. Soc. Ser. B 261, BRANTON, D., BULLIVANT, S., GILULA, N. B., KARNOVSKY, M. J., MOOR, H., MUHLETHALER, K., NORTHCOTE, D. H., PACKER, L., SATIR, B., SATIR, P., SPETH, V., STAEHELIN, L. A., STEERE R. L. & WEINSTEIN, R. S. (1975). Freeze-etching nomenclature. Science, N.Y. 190, DECKER, R. S. & FRIEND, D. S. (1974). Assembly of gap junctions during amphibian neurulation. J. Cell Biol. 62, FRIEND, D. S. & FAWCETT, D. W. (1974). Membrane differentiation in freeze-fractured mammalian sperm. J. Cell Biol. 63, KREUTZICER, G. O. (1968). Freeze-etching of intercellular junctions in mouse liver. In Proc. 26th Meet. Electron Micros. Soc. America, pp Baton Rouge, La.: Claitor's Publishing Division.
5 Pore-like structures in membranes 161 McNurr, N. S. & WEINSTEIN, R. S. (1970). The ultrastructure of the nexus. A correlated thinsection and freeze-cleave study. J. Cell Biol. 47, MCNUTT, N. S. & WEINSTEIN, R. S. (1973). Membrane ultrastructure at mammalian intercellular junctions. Progr. Biophys. molec. Biol. 26, MOOR, H. & MUHLETHALER, K. (1963). Fine structure in frozen-etched yeast cells. J. Cell Biol. 17, PAYTON, B. W., BENNETT, M. V. L.& PAPPAS, G. (i969).permeabilityandstructureof junctional membranes at an electrotonic synapse. Science, N.Y. 166, REVEL, J. P. & KARNOVSKY, M. J. (1967). Hexagonal array of subunits in intercellular junctions of the mouse heart and liver. J. Cell Biol. 23, C7-C12. SINGER, S. J. (1974). The molecular organization of membranes. A. Rev. Biochem. 43, SINGER, S. J & NICOLSON, G. L. (1972). The fluid mosaic model of the structure of cell membranes. Science, N.Y. 175, SOLOMON, A. K. (1968). Characterization of biological membranes by equivalent pores. J. gen. Physiol. 51, 335S-364S. VAIL, W. J., PAPAHADJOPOULOS, D. & MOSCARELLO, M. A. (1974). Interaction of a hydrophobic protein with liposomes: evidence for particles seen in freeze-fracture as being proteins. Biochim. biophys. Ada 345, WOODBURY, J. W. (1965). The cell membrane: ionic and potential gradients and active transport. In: Physiology and Biophysics, igth edn (ed. Th. C. Ruch & H. D. Patton), pp Philadelphia: Saunders. (Received 13 September 1976)
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