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PubMed1977

Permeability of amino acids into liposomes.

1. A simple and rapid assay for the measurement of permeability of amino acids into liposome membrane was carried out by using the liposomes trapping D-amino acid oxidase (D-amino acid: O2 oxidoreductase (deaminating), EC 1.4.3.3) inside the membrane. 2. Permeability of amino acids into liposomes depended on the lipid composition of the membrane. Permeability of amino acids into phosphatidylcholine-cholesterol liposomes depended critically on temperature. 3. Permeability also depended on the structure of amino acids. The order of permeability was norvaline greater than isoleucine greater than leucine greater than phenylalanine greater than tryptophan greater than methionine greater than tyrosine, valine greater than threonine greater than serine greater than alanine greater than glycine.

Amino Acids↗
PubMed1980

Inhibition of anion and glucose permeabilities by anesthetics in erythrocytes. The mechanisms of action of positively and negatively charged drugs.

(1) The mode of action of anesthetics as inhibitors of Cl- and glucose transports in human red cells was studied. The term anesthetic is taken in its broad meaning as defined by Seeman (Seeman, P. (1972) Pharmacol. Rev. 24, 583-655) and covers anionic and cationic liposoluble compounds which reversibly block the rising phase of the action potential, without effect on the resting membrane potential. (2) Phenothiazine derivatives were chosen as prototypes of anesthetics because they represent a set of compounds having the same basic chemical structure, the phenothiazine ring, but with either a positive or a negative charge. (3) The Cl- self-exchange is inhibited by both cationic and anionic derivatives. However, to obtain the same level of inhibition, it is necessary to use a concentration 10-100 times higher with cationic than with anionic drugs. (4) At a concentration which inhibits Cl- permeability, cationic derivatives induce a very strong morphological change (cup-shaped cells: stomatocytes or spherostomatocytes) and protect erythrocytes against osmotic hemolysis, signifying that the membrane is fully expanded. Conversely, with anionic derivatives, inhibition occurs at a concentration which does not induce any apparent shape change or protect against osmotic hemolysis: there is no significant membrane expansion. (5) Glucose permeability, measured by glucose exit, is inhibited by cationic and anionic phenothiazine, but always at a concentration which fully expands the membrane as indicated by morphological changes and anti-hemolytic effects. It is interesting to point out that whilst glucose exit shows inhibition by cationic derivatives, glucose exchange flux is scarcely altered. (6) It is concluded that cationic and anionic anesthetics are general inhibitors of transmembrane solute movements involving a facilitated-diffusion process. However, the mechanism of inhibition is not identical for all: inhibition of glucose permeability by anionic and cationic anesthetics, as well as inhibition of Cl- permeability by cationic anesthetics may be of a non-specific nature and result from their interaction with the bilayer (this indirect effect is discussed); on the other hand, inhibition of Cl- permeability by anionic anesthetics may result from a specific perturbation of the transport mechanism according to recent evidence in some cases (Cousin, J.L. and Motais, R. (1979) J. Membrane Biol. 46, 125-153; Zaki, L., Ruffing, W. Gärtner, E.M., Fasold, H., Motais, R. and Passow, H. (1977) 11th FEBS Meeting, Copenhagen, A4 17-671.

Anions↗
PubMed1981

Permeability of reconstituted sarcoplasmic reticulum vesicles. Reconstitution of the K+, Na+ channel.

Permeability properties of reconstituted rabbit skeletal muscle sarcoplasmic reticulum vesicles were characterized by measuring efflux rates of [3H]inulin, [3H]choline+, 86Rb+, and 22Na+, as well as membrane potential changes using the voltage-sensitive probe, 3,3'-dipentyl-2,2'-oxacarbocyanine. Native vesicles were dissociated with deoxycholate and were reconstituted by dialysis. Energized Ca2+ accumulation was partially restored. About 1/2 of the reconstituted vesicles were found to be 'leaky', i.e., permeable to choline+ of Tris+ but not to inulin. The remaining reconstituted vesicles were 'sealed', i.e., impermeable to choline+, Tris+ and inulin. Sealed reconstituted vesicles could be further subdivided according to their K+, Na+ permeability. About 1/2, previously designated Type I, were readily permeable to K+ and Na+, indicating the presence of the K+, Na+ channel of sarcoplasmic reticulum. The remaining sealed vesicles (Type II) formed a permeability barrier to K+ and Na+, suggesting that they lacked the K+, Na+ channel. These studies show that the K+, Na+ channel of sarcoplasmic reticulum can be solubilized with detergent and reconstituted with retention of activity. Furthermore, our results suggest that part or all of the decreased Ca2+-loading efficiency of reconstituted vesicles may be due to the presence of a significant fraction of leaky vesicles.

Animals↗
PubMed1982

Proton permeability of liposomes from natural phospholipid mixtures.

A method to determine the proton permeability coefficient of phospholipid membrane with the fluorescent probe pyranine is described. Very high proton permeability coefficients of liposomes from natural extracts are measured with great accuracy. The proton permeability appears to be linearly related to the fluidity of the bilayers. This relation as well as the comparison of the activation energies of proton permeability and fluidity support the hypothesis (Nichols J.W. and Deamer D.W. (1980) Proc. Natl. Acad. Sci. USA 77, 2038--2042) of a transfer process along a network of hydrogen bonded water molecules. It is suggested that the common lipid characteristics of biological membranes (net surface charge and unsaturation) favor a high proton permeability.

Carbonyl Cyanide m-Chlorophenyl Hydrazone↗
PubMed1982

[NMR studies of glycerol permeability in lipid vesicles, erythrocytes and the alga Dunaliella].

Glycerol diffusional permeabilities through the cytoplasmic cell membrane of Dunaliella salina, the cell envelope of pig erythrocyte and egg phosphattidylcholine vesicles were measured by NMR spectroscopy employing the spin-echo method and nuclear T1 relaxation. The following permeability coefficients (P) and corresponding enthalpies of activation (delta H not equal to ) were determined for glycerol at 25 degree C: for phosphatidylcholine vesicles 5 . 10-6 cm/s and 11 +/- 2 kcal/mol; for pig erythrocytes 7 . 10-8 cm/s and 18 +/- 3 kcal/mol, respectively; for the cytoplasmic membrane of D. salina the permeability at 17 degrees C was found to be exceptionally low and only a lower limit (P less than 5 . 10-11 cm/s) could be calculated. At temperatures above 50 degree C a change in membrane permeability occurred leading to rapid leakage of glycerol accompanied by cell death. The data reinforce the notion that the cytoplasmic membrane of Dunaliella represents a genuine anomaly in its exceptional low permeability to glycerol.

Animals↗
PubMed1982

Osmotic permeabilities across corneal endothelium and antidiuretic hormone-stimulated toad urinary bladder structures.

Osmotic permeabilities of several epithelial structures have been determined with novel optical procedures based on specular microscopy. The osmotic permeabilities of several tissue layers were determined by continuously monitoring the position of the apical tissue borders while an osmotic flow was imposed across those layers. The values found were (in micrometer/s; mean +/- SE): corneal epithelium, 137 +/- 30 (n = 5): antidiuretic hormone stimulated toad bladder, 429 +/- 64 (n = 6); and corneal endothelium, 711 +/- 34 (n = 7). In addition, the osmotically-induced transient change in thickness of the corneal endothelial cells was determined with the help of a computer, and the apparent osmotic permeability measured for the apical membrane was 1420 +/- 160 micrometer/s (n = 5). It is concluded that the osmotic permeability across the endothelial layer is sizably larger than had been previously detected and that osmotic flows across such layer largely traverse the cellular membranes. With osmotic permeability values (per unit of cell membrane area) as large as presently reported, isotonic fluid transport by epithelia can be explained simply on the basis of local osmotic gradients.

Animals↗
PubMed1982

Effect of retinol and retinoic acid on permeability, electrical resistance and phase transition of lipid bilayers.

Retinol and retinoic acid have been incorporated into the artificial membrane systems, planar bimolecular lipid membranes and liposomes, and their effects on several membrane parameters have been measured. 1. Retinol and retinoic acid increased the permeability of egg lecithin liposomes to K+, I- and glucose when incorporated into the membranes at levels as low as 0.5 membrane mol%. Retinoic acid influenced permeability more than did retinol for each of the solutes tested. 2. Retinol and retinoic acid both decreased the electrical resistance of egg lecithin-planar bimolecular lipid membranes from 0.5 to 8 membrane mol%. Retinoic acid effected a larger change than did retinol. 3. Retinol and retinoic acid increased the permeability of dimyristoylphosphatidylcholine and dipalmitoylphosphatidylcholine liposomes to water at 1.0 and 3.0 membrane mol%. A larger effect on water permeability was measured for retinoic acid than for retinol. 4. Retinol and retinoic acid at 1.0 and 3.0 membrane mol% were shown to lower the phase-transition temperature of liposomes composed of dimyristoylphosphatidylcholine or dipalmitoylphosphatidylcholine. Phase-transition temperatures were monitored by abrupt changes in water permeability and liposome size associated with the transition. Retinoic acid lowered the phase-transition temperature of dimyristoylphosphatidylcholine liposomes more than did retinol, while both retinoids had almost the same effect on dipalmitoylphosphatidylcholine liposomes.

Dimyristoylphosphatidylcholine↗
PubMed1983

Effects of sulfhydryl and other reagents on the diffusional permeability of dog erythrocytes to small solutes.

The effects of p-chloromercuriphenylsulfonic acid (PCMBS), 5,5'-dithiobis (2-nitrobenzoic acid) (DTNB), phloretin and thiourea on the diffusional permeability of dog erythrocytes to tritiated water and to small 14C-labeled lipophilic and hydrophilic solutes were measured at 37 degrees C by means of the linear diffusion technique. Permeability to 3HHO was significantly decreased by PCMBS but was not affected by the other reagents. The permeability to the small hydrophilic solutes acetamide and urea was decreased by phloretin and thiourea but only the permeability to acetamide was reduced to a statistically significant extent by PCMBS. The permeability to the lipophilic solutes methanol, ethanol and antipyrine was not affected by any of these agents. We interpret these results as an indication that the small lipophilic solutes probably move through lipid areas, that the small hydrophilic solutes probably move through protein associated areas in the erythrocyte membrane and that pathways for the small hydrophilic solutes are distinct from those for water. While the pathways for water may be associated with membrane protein they do not appear to be associated specifically with band 3 protein as has been suggested for human erythrocytes. Diffusional water movement through the dog erythrocyte occurs by two distinct pathways.

4-Chloromercuribenzenesulfonate↗
PubMed1985

Interaction of the polyene antibiotic etruscomycin with large unilamellar lipid vesicles: binding and proton permeability inducement.

The effect of the polyene antibiotic etruscomycin on the permeability of large unilamellar lipid vesicles was investigated. Proton leakage was induced in egg-yolk phosphatidylcholine (EPC) vesicles only when sterol was present in the membrane; the extent of leakage was limited. High etruscomycin/lipid ratios (R) were necessary (R greater than 0.1). Higher percentages of sterol increased the permeability, slightly more strongly for ergosterol than for cholesterol. Dipalmitoylphosphatidylcholine (DPPC) vesicles were more sensitive to permeability inducement, even in the absence of sterol in the bilayer (inducement for R greater than 0.06). The interactions of etruscomycin with the vesicles were examined by circular dichroism, fluorescence and 31P-NMR. In the range of antibiotic concentration where permeability was induced, R greater than 0.1 for EPC vesicles, R greater than 0.06 for DPPC vesicles, etruscomycin exhibited characteristic circular dichroism spectra independent of the presence of sterol. Under the same conditions, 31P-NMR and fluorescence studies indicated a destruction or a fusion of the vesicle bilayer. At lower etruscomycin concentrations (R less than 0.03), the etruscomycin circular dichroism spectra were different, indicating that the interaction with membranes containing ergosterol differed from that with membranes containing cholesterol. From correlating the increase in fluorescence intensity with this interaction, as well as from exchange experiments, it was inferred that etruscomycin at a low antibiotic/lipid ratio is more strongly bound to ergosterol-containing vesicles than to cholesterol-containing vesicles. These results and their comparison with the results obtained with other polyene antibiotics indicate that at low R etruscomycin resembles amphotericin rather than filipin in its preferential binding to ergosterol-containing vesicles. At higher R, that is in conditions where permeability is induced, the selectivity is different. The corresponding mechanism seems not to involve the formation of an etruscomycin-sterol channel, since the hydrophobic chain of the complex would be too short to form a channel.

Antifungal Agents↗
PubMed1987

Alterations by saponins of passive Ca2+ permeability and Na+-Ca2+ exchange activity of canine cardiac sarcolemmal vesicles.

Saponins can both permeabilize cell plasma membranes and cause positive inotropic effects in isolated cardiac muscles. Different saponins vary in their relative abilities to cause each effect suggesting that different mechanisms of action may be involved. To investigate this possibility, we have compared the effects of seven different saponins on the passive Ca2+ permeability and Na+-Ca2+ exchange activity of isolated canine cardiac sarcolemmal membranes. Saponins having hemolytic activity reversibly increased the passive efflux of Ca2+ from sarcolemmal vesicles preloaded with 45Ca2+ with the following order of potency: echinoside-A greater than echinoside-B greater than holothurin-A greater than holothurin-B greater than sakuraso-saponin. Ginsenoside-Rd and desacyl-jego-saponin, which lack hemolytic activity, had no significant effect on this variable. The saponins also stimulated Na+-Ca2+ exchange activity measured as Na+-dependent Ca2+ uptake by sarcolemmal vesicles. Ginsenoside-Rd and desacyl-jego-seponin, which did not affect passive Ca2+ permeability, stimulated the uptake, while in contrast, echinoside-A and -B only slightly increased or decreased this latter variable. Thus, the abilities of these compounds to enhance Na+-Ca2+ exchange activity seem to be inversely related to their abilities to increase the Ca2+ permeability. Effects by the echinosides on Na+-Ca2+ exchange may be masked by the loss of Ca2+ from the vesicles due to the increased permeability. These results suggest that the saponins interact with membrane constituent(s) that can influence the passive Ca2+ permeability and the Na+-Ca2+ exchange activity of cardiac sarcolemmal membranes.

Animals↗
PubMed1988

Permeability of inner mitochondrial membrane and oxidative stress.

The mechanism of increase in the inner membrane permeability induced by Ca2+ plus Pi, diamide and hydroperoxides has been analyzed. (1) The permeability increase is antagonized by oligomycin and favoured by atractyloside. The promoting effect of atractyloside is strongly reduced if the mitochondria are simultaneously treated with oligomycin. (2) Addition of the free-radical scavenger, butylhydroxytoluene, results in a complete protection of the membrane with respect to the permeability increase. (3) Although membrane damage and depression of the GSH concentration are often associated, there is no direct correlation between extent of membrane damage and concentration of reduced glutathione. Abolition of the permeability increase by butylhydroxytoluene or by oligomycin is not accompanied by maintenance of a high GSH concentration in the presence of diamide or hydroperoxides. The membrane damage induced by Ca2+ plus Pi is not accompanied by a depression of the GSH concentration. (4) It is proposed that a variety of processes causing an increased permeability of the inner mitochondrial membrane merge into some ultimate common steps involving the action of oxygen radicals.

Adenosine Triphosphate↗
PubMed1989

Lipid permeability of the intestinal microvillus membrane may be modulated by membrane fluidity in the rat.

Fatty acids and cholesterol permeate across the intestinal microvillus membrane at rates dictated by the hydrophobicity of the permeating lipid and the permeability properties of the microvillus membrane. A theory has evolved suggesting that the chemical composition and physical properties of the microvillus membrane are important in determining microvillus membrane lipid permeability in vivo. This communication reports a test of this hypothesis. To compare in vivo membrane lipid permeability within the same intestinal region, but under conditions were membrane physical properties were radically altered, rats were fed an inhibitor of cholesterol synthesis. This resulted in the replacement of 87-90% of membrane cholesterol with its' precursor, 7-dehydrocholesterol. Marked changes in membrane physical properties were observed, including a reduction in the static and dynamic component of membrane fluidity within the jejunal microvillus membrane. These changes were limited primarily to the outer regions of the bilayer. Associated with these alterations was a pronounced reduction in membrane lipid permeability. Therefore, microvillus membrane lipid permeability, in vivo, appears to be correlated with physical properties of the bilayer, especially those of the superficial regions.

Animals↗
PubMed1990

The apparent permeability coefficient for proton flux through phosphatidylcholine vesicles is dependent on the direction of flux.

A dioleoylphosphatidylcholine unilamellar vesicle model system was used to determine proton permeability. The fluorescence of the pH reporter group, pyranine, trapped within vesicles with a difference in pH across the bilayer, was digitized and analyzed with numerical integration. When H+ flux was initiated by the acidification of the external buffer (acid jump), the apparent H+ permeability was found to be a linear function of the reciprocal of the internal H+ concentration with the slope inversely proportional to the initial size of the H+ gradient. When flux was initiated by the alkalinization of the external buffer (base jump), the apparent permeability coefficient was constant for each external H+ concentration. However, the value of the apparent permeability was linearly dependent on the reciprocal of the external H+. The possibility that carbonates (carbon dioxide, carbonic acid, bicarbonate and carbonate) could be acting as proton carriers was tested by adding millimolar concentrations of bicarbonate to solutions greatly reduced in carbonates. The slopes of the graphs of apparent permeability coefficient vs. reciprocal H+ were linear functions of added bicarbonate concentration for both acid and base jump conditions. These observations were interpreted in terms of a model suggesting that carbonic acid or carbon dioxide together with bicarbonate was an efficient proton carrier across phospholipid bilayers.

Arylsulfonates↗
PubMed1992

Involvement of cytoskeletal proteins in the barrier function of the human erythrocyte membrane. III. Permeability of spectrin-depleted inside-out membrane vesicles to hydrophilic nonelectrolytes. Formation of leaks by chemical or enzymatic modification of membrane proteins.

Spectrin-depleted inside-out vesicles (IOV's) prepared from human erythrocyte membranes were characterized in terms of size, ground permeability to hydrophilic nonelectrolytes and their sensitivity to modification by SH reagents, DIDS and trypsin. IOV's proved to have the same permeability of their lipid domain to erythritol as native erythrocytes, in contrast to resealed ghosts (Klonk, S. and Deuticke, B. (1992) Biochim. Biophys. Acta 1106, 126-136 (Part I in this series)), which have a residual leak. On the other hand, IOV's have a slightly elevated permeability for mannitol and sucrose, nonelectrolytes which are almost (mannitol) or fully (sucrose) impermeant in the native membrane. These increased fluxes, which have a high activation energy and can be stimulated by phloretin, are, however, also much smaller than the corresponding leak fluxes observed in resealed ghosts. In view of these differences, formation of IOV's can be concluded to go along with partial annealing of barrier defects persisting in the erythrocyte membrane after preparation of resealed ghosts. Oxidation of SH groups of the IOV membrane by diamide produces an enhancement of permeability for hydrophilic nonelectrolytes which is much less pronounced than that induced by a similar treatment of erythrocytes or ghosts (Klonk, S. and Deuticke, B. (1992) Biochim. Biophys. Acta 1106, 126-136 (Part I in this series)). Moreover, proteolytic treatment of the vesicle membrane, although leading to a marked digestion of integral membrane proteins, only induces a minor, saturating increase of permeability, much lower than that in trypsinized resealed ghosts (Klonk, S. and Deuticke, B. (1992) Biochim. Biophys. Acta 1106, 137-142 (Part II of this series)). Since absence of the cytoskeletal proteins, spectrin and actin, is the major difference between IOV's and resealed ghosts, these results may be taken as further evidence for a dependence of the barrier properties of the erythrocyte membrane bilayer domain on its interaction with cytoskeletal elements. In contrast, these barrier properties seem to be rather insensitive to perturbations of integral proteins.

Cell Membrane Permeability↗
PubMed1992

Permeability of lipid bilayers to amino acids and phosphate.

Permeability coefficients for amino acid classes, including neutral, polar, hydrophobic, and charged species, were measured and compared with values for other ionic solutes such as phosphate. The rates of efflux of glycine, lysine, phenylalanine, serine and tryptophan were determined after they were passively entrapped in large unilamellar vesicles (LUVs) composed of egg phosphatidylcholine (EPC) or dimyristoylphosphatidylcholine (DMPC). The following permeability coefficients were obtained for: glycine, 5.7 x 10(-12) cm s-1 (EPC), 2.0 x 10(-11) cm s-1 (DMPC); serine, 5.5 x 10(-12) cm s-1 (EPC), 1.6 x 10(-11) cm s-1 (DMPC); lysine, 5.1 x 10(-12) cm s-1 (EPC), 1.9 x 10(-11) cm s-1 (DMPC); tryptophan, 4.1 x 10(-10) cm s-1 (EPC); and phenylalanine, 2.5 x 10(-10) cm s-1 (EPC). Decreasing lipid chain length increased permeability slightly, while variations in pH had only minor effects on the permeability coefficients of the amino acids tested. Phosphate permeability was in the range of 10(-12)-10(-13) cm s-1 depending on the pH of the medium. The values for the polar and charged amino acids were surprisingly similar to those previously measured for monovalent cations such as sodium and potassium, which are in the range of 10(-12)-10(-13) cm s-1, depending on conditions and the lipid species used. This observation suggests that the permeation rates for the neutral, polar and charged amino acids are controlled by bilayer fluctuations and transient defects, rather than partition coefficients and Born energy barriers. The results are relevant to the permeation of certain peptides into lipid bilayers during protein translocation and membrane biogenesis.

Amino Acids↗
PubMed1994

Developmental changes of renal brushborder membrane ionic permeability.

Renal brush-border membrane vesicles (BBMV) show an age-dependent increase in height of the Na(+)-gradient driven overshoot for glucose and proline uptake. Conversely, early uptake of 22Na+ is more rapid in BBMV from kidney of 7-day-old vs. adult rats. To understand the mechanisms responsible for these observations, ionic permeability characteristics of BBMV from different aged animals were determined using an electrical potential sensitive fluorescent dye, diS-C3(5). Absolute and relative ionic permeabilities were determined after a 3-h incubation in 100 mM KCl. Intravesicular K+ ([K+]in), a measure of absolute K+ permeability, was calculated from the extravesicular K+ at which valinomycin produced no potential difference (PD). [K+]in was significantly lower in vesicles from 7-day, compared to adult (P < 0.01). While Cl- permeability, relative to that of K+ was similar, PNa+/PK+ decreased significantly with age (P < 0.05, 7 day vs. adult). In the presence of an inwardly directed NaCl gradient, the lower PNa+ relative to PCl- of the adult vesicles would result in a less positive intravesicular charge, which would therefore augment Na(+)-solute co-transport. Fluorescence polarization studies also show that lipids from BBM vesicles of 7-day-old rats are more fluid than those from adult. These differences are likely due to developmental lipid compositional changes, which influence membrane transport and permeability characteristics. These findings would explain, in part, the age-dependent alterations of renal BBMV solute transport.

Aging↗
PubMed1976

DNA synthesis and repair in permeable cells of Micrococcus radiodurans.

Cells permeable to deoxyribonucleoside triphosphate were prepared from Micrococcus radiodurans, and DNA synthesis and rejoining of strand scissions induced by gamma-rays were investigated. DNA synthesis was stimulated by ATP at an optimal concentration of 1mM. This reaction requires four deoxyribonucleoside triphosphates and MgCl2. NAD inhibited the reaction, but no rejoining of primer DNA was observed. Even in the presence of NAD, DNA which was synthesized in the unirradiated permeable cells had a peak molecular weight of only 1.3 - 10(6). DNA synthesis was stimulated by irradiation of the permeable cells with gamma-rays, but this stimulatory effect was eliminated by the addition of NAD. Both primer and synthesized DNA in the irradiated permeable cells were rejoined in vitro in the presence of NAD and deoxyribonucleoside triphosphates, while those in the unirradiated permeable cells were not rejoined.

Biological Transport↗
PubMed1990

Atrial natriuretic peptide regulation of endothelial permeability is mediated by cGMP.

Previous studies in our laboratory showed that ANP inhibits increases in endothelial monolayer permeability to macromolecules induced by thrombin. In this present study, we investigated the second messenger system involved in the influence of ANP on monolayer permeability. In bovine aortic endothelial cells (BAEC), ANP (100 nM) caused increased cGMP levels which were measurable at 30 sec and maximal at 3 min. Addition of 8-bromo cGMP (1 mM) to BAEC monolayers mimicked the actions of ANP by inhibiting thrombin- mediated increases in permeability to [125I]-labeled bovine serum albumin. Inhibition of increases in permeability by lower concentrations of ANP was enhanced by the cGMP-selective phosphodiesterase inhibitor, M&B 22948 (100 microM). The use of ANP structural analogs which stimulate cGMP production (AP III or BNP) prevented thrombin-induced increases in monolayer permeability, whereas AP-I, which does not increase cGMP levels, was ineffective.

3',5'-Cyclic-AMP Phosphodiesterases↗