Thermotropic fluid → ordered "discontinuous" phase separation in microsomal lipids of Tetrahymena. An x-ray diffraction study

Wunderlich, Frank; Kreutz, W.; Mahler, Peter A.; Ronai, Adam; Heppeler, Gerlinde

doi:10.1021/bi00603a032

Cited by 70 publications

(29 citation statements)

References 35 publications

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“…By 1974, studies on the effects of temperature on membrane behavior had led investigators to propose the presence of "clusters of lipids" in membranes (2), and by the following year data were obtained that suggested that these clusters might be "quasicrystalline" regions surrounded by more freely dispersed liquid crystalline lipid molecules (3). By 1978, this idea had been refined from "rigid liquid crystalline" clusters to "lipids in a more ordered state" (4).…”

mentioning

confidence: 99%

The challenge of lipid rafts

Pike

2009

Journal of Lipid Research

451

351

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The Singer-Nicholson model of membranes postulated a uniform lipid bilayer randomly studded with floating proteins. However, it became clear almost immediately that membranes were not uniform and that clusters of lipids in a more ordered state existed within the generally disorder lipid milieu of the membrane. These clusters of ordered lipids are now referred to as lipid rafts. This review summarizes current thinking on the nature of lipid rafts focusing on the role of proteomics and lipidomics in understanding the structure of these domains. It also outlines the contribution of single-molecule methods in defining the forces that drive the formation and dynamics of these membrane domains.-Pike, L. J. A major step forward in our understanding of the structure of biological membranes was the publication by Singer and Nicolson (1) in 1972 of the fluid mosaic model of membranes. The model described the membrane as a primarily lipid matrix with randomly distributed proteins. The ink had barely dried on this landmark paper before experimental evidence was obtained that suggested that the uniformly random distribution of proteins and lipids envisioned by Singer and Nicholson was probably inaccurate. By 1974, studies on the effects of temperature on membrane behavior had led investigators to propose the presence of "clusters of lipids" in membranes (2), and by the following year data were obtained that suggested that these clusters might be "quasicrystalline" regions surrounded by more freely dispersed liquid crystalline lipid molecules (3). By 1978, this idea had been refined from "rigid liquid crystalline" clusters to "lipids in a more ordered state" (4).The concept of lipid domains in membranes was formalized in 1982 by Karnovsky et al. (5), who observed heterogeneity in the lifetime decay of 1,6-diphenyl-1,3,5-hexatriene, indicating multiple phases in the lipid environment of the membrane. These workers also investigated the functional effect of altering membrane structure by the addition of specific fatty acids, and presciently, by the depletion of cholesterol. They closed their manuscript with a series of questions that were raised by the "concept of the organization of the lipid components of membranes into domains." Their questions are worth reiterating because almost 3 decades later they remain major challenges in the study of the structures that we have come to call lipid rafts. 1) Do specific membrane proteins reside in specific lipid domains, and can perturbation of the specific domain structure affect protein structure and function? 2) Do lipophilic molecules and drugs preferentially partition and segregate into specific domains rather than into a bulk lipid phase, and may such unique partitioning predicate specific functional effects? 3) What forces underlie the formation, maintenance, and fluctuation of lipid domains? 4) Because the very concept of domains implies domain boundaries or interfaces, what is the possible biological significance of such interfaces?In this review, I will summarize rece...

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confidence: 99%

The challenge of lipid rafts

Pike

2009

Journal of Lipid Research

451

351

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“…This implies that the far more complex mixture in biological membranes may form coexisting lipid domains of distinct chemical and physical properties. Evidence for heterogeneity of lateral organization has been documented by electron microscopy (Hui and Parsons, 1975), X-ray diffraction (Wunderlich et al 1978), lateral diffusion measurements (Bultmann et al, 1991), differential scanning calorimetry (Wolf et al, 1990), spin-label measurement (Stier and Sackmann, 1973), spectroscopic techniques (Klausner et al, 1980), and digitized fluorescence microscopy (Rodgers and Glaser, 1991). Real membranes may differ from each other in the number of immiscible phases as well as in the distribution pattern of the different domains, Since during membrane reorganizations both lipid microdomain structures and macrocompartmentation can be involved (Tocanne et al, 1989), systems situated near a transition boundary in the phase diagram can be affected dramatically by a small change in chemical composition or some other critical physical parameter.…”

Section: Discussionmentioning

confidence: 99%

Hypo-osmotic shock induces an osmolality-dependent permeabilization and structural changes in the membrane of carp sperm.

Márián¹,

Krasznai²,

Balkay³

et al. 1993

J Histochem Cytochem.

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We carried out spectrofluorimetric and flow cytometric measurements to investigate the effect of hypo-osmotic shock on cell membranes of common carp sperm. The time course of the permeability of the sperm cell membrane, as monitored by DNA-related propidium iodide (PI) fluorescence, was followed for 30 min after dilution of semen in hypoosmotic environments of different ionic strengths. Specaofluorimetric measurements indicated a continuous inaease in the toml PI emission intensity of a sperm suspension. Cellb y 4 flow cytometric measurements suggested that the per- min. This equilibrium fraction of cells with a PI-permeable

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“…At present we only know that neutral lipids are minor membrane constituents (e.g. = 15% of total lipids in microsomal membranes of Tetrahymena [17]), and that they exert a slight disorganizing effect on the bilayer stacking of phospholipids extracted from Tetrahymena microsomes as shown recently by low-angle X-ray diffraction [29].…”

Section: Lowered Lipid Clustering-temperature In Expanded Nuclear Memmentioning

confidence: 94%

“…also [ll]). According to our present concept [23,29] such thermotropic changes in nuclear membranes are induced by a clustering of ordered lipid domains occurring within a broad thermotropic fluid e ordered lipid phase separation. Specifically, our concept, based on studies using electron spin resonance, fluorescence spectroscopy, thermal calorimetry, proton nuclear magnetic resonance, small-angle and wide-angle X-ray diffraction, proposes that fluid and ordered lipids coexist in Tetrahymena endomembranes at the cells' growth temperature, i.e.…”

Section: Tetrahymena Grown At 28 " C or 18°cmentioning

confidence: 98%

Suppression of Thermotropic Lipid Clustering in Tetrahymena Nuclear Membranes upon Ca²⁺/Mg²⁺ Induced Membrane Contraction

Giese

Fromme

Wunderlich

1979

European Journal of Biochemistry

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Nuclear membranes surrounding the macronuclei isolated from Tetrahymena cells grown at either 28 "C or 18 'C are induced to expand or contract laterally by Ca2+/Mg2+ (3/2) in final concentrations of 1 mM or 5 mM, respectively. Only expanded nuclear membranes are temperature-responsive as revealed by freeze-etch electron microscopy and electron spin resonance using 5-doxylstearic acid as a spin label.In expanded nuclear membranes from growth at 28 "C, electron spin resonance detects, upon lowering the temperature, a biphasic decrease of the lipid fluidity in terms of 2T11 with a discontinuity at z 17 "C. In this temperature range, freeze-etch electron microscopy reveals an increase in the number of nuclear membrane fracture faces with smooth areas. We ascribe this response to a clustering of ordered lipid domains within a broad thermotropic fluid-+ ordered lipid phase separation ) Biochemistry, 17, 2005 Expanded nuclear membranes from growth at 18 'C shift their lipid clustering temperature down to z 12 "C. Their lipid fluidity (~T I I )is increased in comparison with the nuclear membranes from growth at 28 "C. This is probably due to an increased fatty acid unsaturation of the polar lipids. Thin-layer-chromatography reveals the following major polar lipids in the nuclei from growth at 18 "C (28 "C): 33.9 % (31.4 %) phosphatidylethanolamine, 14.2 % (13.4 %) phosphatidylethylamine, 22.5% (18.0%) unidentified phospholipid, 21.4% (19.1 %) phosphatidylcholine, and 6.1 (10.4%) ceramide-phosphonoethylamine. The major fatty acids are mainly even-numbered ranging between C12 and CIS as analyzed by gas chromatography. The 18"-nuclei (28O-nuclei) contain 67.1 % (60.4%), 74.5 (68.4 x), and 32.3 % (43.5 %) unsaturated fatty acids in their total lipids, polar lipids, and neutral lipids, respectively. The individual phospholipids, except phosphatidylcholine and ceramidephosphonoethylamine, are more unsaturated in the nuclei from growth at 18 "C.Contracted nuclear membranes from growth at 28 "C and 18 "C suppress thermotropic lipid clustering. They reveal an apparent higher lipid fluidity and percentage of fracture faces with smooth areas than the corresponding expanded nuclear membranes at 28 "C and 18 "C, respectively. The lipid clustering suppression is interpreted as being due to a change in lipid packing which in turn is induced by a Ca2+/Mg2+-induced contraction of the Ca2+/Mg2+-sensitive nucleoskeleton proteins associated with nuclear membranes.Biomembranes are temperature-responsive. In particular, the membrane lipids can undergo thermotropic fluid ( = disordered) + ordered phase transitions (for comprehensive reviews see e.g. [I, 21). These transitions depend on a variety of factors which include the nature of the fatty acids and head groups of polar lipids, pH changes, the cholesterol content, etc. For instance, an increased unsaturation of the fatty acid residues in polar lipids generally shifts the transition to lower temperatures. Moreover, increasing complexity of the lipid composition normally causes an increase ...

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Thermotropic fluid → ordered "discontinuous" phase separation in microsomal lipids of Tetrahymena. An x-ray diffraction study

Cited by 70 publications

References 35 publications

The challenge of lipid rafts

The challenge of lipid rafts

Hypo-osmotic shock induces an osmolality-dependent permeabilization and structural changes in the membrane of carp sperm.

Suppression of Thermotropic Lipid Clustering in Tetrahymena Nuclear Membranes upon Ca²⁺/Mg²⁺ Induced Membrane Contraction

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Thermotropic fluid → ordered "discontinuous" phase separation in microsomal lipids of Tetrahymena. An x-ray diffraction study

Cited by 70 publications

References 35 publications

The challenge of lipid rafts

The challenge of lipid rafts

Hypo-osmotic shock induces an osmolality-dependent permeabilization and structural changes in the membrane of carp sperm.

Suppression of Thermotropic Lipid Clustering in Tetrahymena Nuclear Membranes upon Ca2+/Mg2+ Induced Membrane Contraction

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Suppression of Thermotropic Lipid Clustering in Tetrahymena Nuclear Membranes upon Ca²⁺/Mg²⁺ Induced Membrane Contraction