Inactive fatty acids are unable to ip- op across the lipid bilayer
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1 Key words : Ftty Institute of Physiology, Deprtment of Membrne Trnsport Biophysics, Acdemy of Sciences of the Czech Republic, V è den í sk è 1083, Abbrevitions : ADIFAB, PII CZ Prgue, Czech Republic Oregon Grdute Institute, Deprtment of Chemistry, Biochemistry nd Moleculr Biology, NW Wlker Rod, Portlnd, OR , USA 2.1. Mesurement of the net H in ux into liposomes 2.3. Mesurement of FA prtitioning between wter nd liposomes : ADIFAB method FEBS FEBS Letters 408 (1997) 161^165 Inctive ftty cids re unble to ip- op cross the lipid bilyer Petr Jezíek ; *, Mrtin Modrinskyè 1;b, Keith D. Grlid b b Received 5 Mrch 1997 Abstrct Free ftty cids (FA) were found which did not cidify liposome interior. This is interpreted s their inbility to rpidly flip-flop cross the lipid bilyer. However, they were ble to prtition in lipids s detected directly using HPLC or from the shift of their equilibrium binding to crylodted intestinl binding protein (ADIFAB) in the presence of vesicles. Vrious bipolr FA, such s 12-hydroxyluric cid, dicrboxylic cids, or FA with benzene ring t the til were found to be inctive in this wy. A phenomenon of shielding, where n dditionl lkyl chin or non-polr group cn restore the flip-flop ctivity, is described. z 1997 Federtion of Europen Biochemicl Societies. H cid ip- op; Ftty cid structure; trnsport 1. Introduction H permebility of pure lipid bilyers (the net H permebility) or of biologicl membrnes (proton lek), ws extensively studied nmely in bioenergetics [1^4], becuse of its inherent importnce in the chemiosmotic theory. One reson for the excessive H permebility of biomembrnes when compred to rti cil lipid bilyers hs been found in the frequent presence of unesteri ed ftty cids (FA) in membrnes [5]. Indeed, long-chin FA re cpble of rpid nonionic ip- op cross biologicl membrnes [6,7]. Nevertheless, FA-induced uncoupling in mitochondri nd other coupling membrnes is not fully explined by this phenomenon either [8]. Skulchev [9] hypothesized tht membrne proteins my conduct FA nions [10] while protonted FA ip bck cross the lipid bilyer, thus crrying H. The FA cycling then mimicks the clssic uncoupler cycling [10]. A question whether both the protonted nd the negtively chrged FA re eqully ble to ip- op cross the lipid bilyer hs been solved. Kmp nd Hmilton [6,7] hve shown tht only the protonted FA cn ip- op very rpidly, while ip- op or di usion of the negtively chrged FA ws severl orders of mgnitude slower. Rtes of ip- op were inferred from the internl cidi ction of liposomes upon ddition of *Corresponding uthor. Fx: (420) E-mil: jezek@sun1.biomed.cs.cz 1 This work ws submitted in prtil fulfillment of requirements for the Ph.D. degree. crylodted intestinl ftty cid binding protein; DOXYL, 4,4-dimethyl-3-oxzolinyloxyl-; FA, free ftty cids (non-esterified); Octyl-POE, octylpentoxy-ethylene; SPQ, 6-methoxy- N-(3-sulfopropyl)quinolinium; TEA, tetrethylmmonium-; TES, N- tris [hydroxymethyl]methyl-2-minoethne-sulfonic cid; TNP, trini- trophenyl- FA. Interestingly, the FA with bulky groups such s 5-DOX- YL-steric cid, 1-pyrenenonnoic cid exhibited the sme fst ip- op with t s [7]. Only ip- op of 12-(9-nthroyloxyl)steric cid proceeded with t12 of 200 s [7]. This study dels with the structurl fetures of FA tht ect the FA's bility to ip- op. We found severl FA derivtives which were unble to ip- op, t lest in the time course of our experiments. Their ip- op rtes, if they exist t ll, must be corresponding to t12 s 30 min. We nmed these FA `inctive' nd recommend them s tool for studying the FA-induced uncoupling. 2. Mteril nd methods The uorescent probes SPQ nd ADIFAB were purchsed from Moleculr Probes (Eugene, OR). Vrious derivtives of ftty cids were purchsed from Sigm nd Fluk (Germny) or Lncster (UK). Egg yolk L-K-phosphtidylcholine, L-K-phosphtidic cid, crdiolipin nd other mterils for liposome preprtion were from the sources s described elsewhere [10]. We used the `SPQ quenching' method of Orosz nd Grlid [11] to monitor the internl cidi ction of vesicles resulting from the ip of dded FA. SPQ is quenched by TES ÿ nion, but not by TES zwitterion, which llows for monitoring of H uxes fter rigorous clibrtion by KOH in the presence of nigericin [11]. FA were dded s Wl liquots of stock solutions in ethnol. Liposomes (25 Wl per ssy) prepred by the detergent (Octyl-POE) removl method with Bio- Beds SM2 contined 84.4 mm TEA-SO 4, mm TES (TEAslt), ph 7.2, nd 0.6 mm TEA-EGTA. Externl medium contined 84.4 mm K 2 SO 4, 50 mm TES (TEA-slt), ph 7.2, nd 1.5 mm TEA- EGTA. Vlinomycin (0.1 WM) ws dded t s in order to test for the H lek Mesurement of FA prtitioning between wter nd liposomes FA (8 Wmol) ws dded to liposomes (40 mg lipids) nd the queous portion of FA ws roughly estimted s the di erence between the originl (totl) mount of FA nd the mount retined in the vesicles fter gel ltrtion on Sephdex G25-300, using spin-columns. The mount of FA ws nlyzed fter smple derivtiztion by phenylcylbromide [12] on n HPLC system (Wters, USA) with n utomted grdient controller, Model 510 pumps, nd W490E bsorbnce detector (242 nm) using 10 WM Nucleosil 250U4 mm column (Mcherey-Ngel, Duëren, Germny) t 46³C. Elution ws done by liner grdient of H 2 O (A)/cetonitrile (B) from 70% B to 100% B t 30 min with ow rte of 2 ml/min. To estimte free FA we used decrese in the slope of plot of the ADIFAB uorescence rtio, R, t 505^432 nm versus totl mount of FA, [FA] totl [13]. Excittion ws set t 477 nm. Experiments were performed on SLM 8000C uorometer. The ssy medium contined 150 mm NCl, 1 mm TEA-EGTA, 10 mm Tris-HCl, ph 8, with 0.2 WM ADIFAB [14,15]. The mount of free FA ws clculted from the experimentlly obtined rtios s described [14,15]: FAŠ free ˆ Kd W Q W R3R0 Rmx3R /97/$17.00 ß 1997 Federtion of Europen Biochemicl Societies. All rights reserved. S (97)
2 P. Jezí ek et l./febs Letters 408 (1997) 161^ Fig. 1. Liposome interior cidi ction is cused by the `ctive' ftty cids but not by the `inctive' ftty cids. Active FA: The upper-hlf contins trces obtined in the presence of 50 WM luric, heptylbenzoic (C 7 bz), 3-hydroxymyristic (3OHC 14 ), steric, 2-hydroxysteric (2OHC 18 ), 12-hydroxysteric 12OHC 18 ) nd dodecyloxybenzoic (C 12 bz) cids. The lower-hlf contins trces obtined in the presence of the inctive FA: 12-hydroxyluric(12OHC 12 ), phenylvleric (PheC 5 ), tetrdecnedioic (C 14 dicoo), dodecnedioic (C 12 dicoo), 9,10,16-trihydroxyplmitic (i.e. leuritic, C 16 trioh) nd 12-minoluric (12NH 2 C 12 ) cids. The bottom trce of the left pnel ws obtined in the presence of ethnol (EtOH) only. The mount of ethnol ws the sme s the mount dded with FA. 0.1 M vlinomycin (Vl) ws dded t 25 or 30 s to test for the H lek. where K d is n equilibrium constnt for binding of the given FA to ADIFAB; Q is the rtio of uorescence t 432 nm t zero nd sturting FA concentrtions; R 0 nd R mx re the corresponding R rtios t zero nd sturting FA concentrtions, respectively. We hd to clculte our own prmeters Q (14.5) nd R mx (5) while using Mrqurdt lgorithm to t the Eq. 4 in [15] onto our dt obtined with oleic cid. This procedure yielded K d vlues to those published for oleic cid [15] binding to ADIFAB (0.39 WM, 0.22 WM, 2 experiments). Eq. 1 hs been used lso to clculte [FA] L free t the equilibrium shifted due to the ddition of liposomes. The respective K ds clculted from the dt of the experiments without liposomes were used. We then evluted the prtition coe cient K p from the dt round K ccording Anel et l. [14] s follows: d K ˆ V p V m W 1 FAŠ L free FAŠ totl3 FAŠ L W free 2 where V /V m is the rtio of volumes of the queous nd membrne phses. V m/v of per 1 mm phospholipids ws used [14]. 3. Results nd discussion In the top hlf of Fig. 1 is illustrted the internl cidi ction in liposomes exposed to K grdient upon ddition of di erent FA t 50 WM concentrtions. An electrochemicl K grdient of pproximtely 180 mv cross the liposoml membrne ws present in ll experiments. Net H ux in vesicles ws monitored vi quenching of SPQ by TES ÿ nion [11]. According to Kmp nd Hmilton [6,7], the cidi ction of vesicle interior cn be interpreted s ip of the protonted FA from the outer to the inner lipid le et of the membrne. The scheme in Fig. 2 shows the possible intermedite non-equilibrium sttes involved nd explins why n internl cidi ction cn be n indiction of FA ip into the inner lipid le et. The ddition of 0.1 WM vlinomycin in the presence of FA cused negligible lkliztion of vesicle interior. The FA-induced H lek is therefore very low [10] nd equl to the H lek existing in the bsence of FA (cf., Fig. 1, bottom trce with only ethnol dded), in spite of the estblished K-di usion potentil of over 180 mv. The lek mgnitudes were between nd 0.03 nmol H s ÿ1 with the inctive FA nd 0.016^0.04 nmol H s ÿ1 with the ctive FA. For comprison, the H lek in the presence of ethnol ws 0.013^0.025 nmol H s ÿ1. Extrpolting to zero mv [16], permebility coe cients
3 P. Jezí ek et l./febs Letters 408 (1997) 161^ Fig. 2. The equilibrium reched upon externl ddition of ftty cid to liposomes. One my simply relize, why interior cidi ction contrdicts to the ip- op of both nionic nd protonted FA molecules. In this cse, hlf of ech species which re originlly distributed ccording cid-bse equilibrium would ip into the inner lipid le et nd the inner cid-bse equilibrium would be set utomticlly if externl ph ws identicl to the internl ph. Hence, there is no need for the interior cidi ction. Di erent sitution occurs, however, when only neutrl FA cn ip- op. In order to estblish equilibrium between the two le ets of bilyer, the mjority of nonionic FA which prtitioned into the outer le et must ip into the inner le et. Consequently, new cid-bse equilibrium must be estblished in the vesicle interior, which leds to the internl H relese. derived from these dt were 1.10 ÿ4 to 4.10 ÿ4 cmws ÿ1.h lek ws signi cntly higher in the presence of 12-hydroxysteric (Fig. 1) nd hexdecnedioic cids (not shown). All physiologiclly bundnt FA nd their derivtives demonstrted the bility to cidify vesicle interior with t12 well below 1 s, s reported [7]. Nevertheless, we found severl FA derivtives (Fig. 1 nd Tble 1), which did not cidify vesicle Fig. 3. Ftty cid binding to ADIFAB in the presence nd bsence of liposome. Binding of FA to ADIFAB ws mesured in the bsence ( lled symbols) nd presence of liposomes (20 WM lipid, open symbols) for () oleic cid; (b) tetrdecnedioic cid; (c) luric cid; (d) 12-hydroxyluric cid. The chrcteric sturtion binding re ected by plot of uorescence rtio, R, t 505^432 nm vs. totl mount of the dded FA, [FA] totl, is shifted upon the ddition of liposomes, thus indicting FA prtitioning into the lipid bilyer. Mesurements were done with the sodium slts in FA in medium contining 150 mm NCl, 1 mm TEA-EGTA, 10 mm Tris-HCl, ph 8, with 0.2 WM ADIFAB [14,15]. The derived K d vlues re listed in the Tble 2, s well s the clculted prtition coe cients K p. interior even if present in concentrtions of 200 WM. No signi cnt chnges in ph in were observed for up to 5 min. We conclude tht these FA were unble to ip- op with signi cnt rte nd we cll them `inctive FA' to distinct them from the `ctive FA' which do posses the bility of fst ip- op. Typiclly, the inctive were FA with polr group in the `til' terminl (g) position. Besides the 12-hydroxyluric cid, the 12-minoluric 2 nd dodecnedioic cids which were inctive in the lurte group, the tetrdecnedioic cid ws inctive in the myristte group. One would ssume presence of 2 NH 2 group hs low polrity, but might form NH 3.
4 P. Jezí ek et l./febs Letters 408 (1997) 161^ Tble 1 Flip- op of vrious ftty cids cross the lipid bilyer s indicted by internl cidi ction in liposomes Compound Extent of ip- op cidi ction hlf-time of ip- op (totl nmol H relesed per 100 nmol FA dded) t12 (s) Active ftty cids Luric (n 7) Hydroxyluric Bromo-luric TNT-luric 2.20 c 4.0 c Myristic Hydroxymyristic Hydroxymyristic (n 3) Plmitic Hydroxyplmitic Steric Hydroxysteric Hydroxysteric Heptylbenzoic (n 4) Dodecyloxybenzoic Hydroxyplmitic Hexdecnedioic b (n 4) Inctive ftty cids with 50 WM d with 200 WM d 12-Hydroxyluric (n 4) s 60 min s 60 min 12-Aminoluric (n 3) 0.04 s 60 min s 30 min Dodecnedioic 0.03 s 2 min s 2 min Tetrdecnedioic s 200 min Phenylhexnoic 0.07 s 200 min s 200 min Phenylvleric (n 3) s 200 min s 200 min 9,10,16-Trihydroxyplmitic 0.03 s 4 min Biphenyl-2-crboxylic 0.08 s 30 min s 200 min 3,3-Diphenylpropionic 0.09 s 200 min s 60 min L-Nphtoic s 30 min s 60 min Experiments were performed in duplicte if not indicted otherwise (n, number of mesurements listed in prentheses) with 50 WM FA dded or with 50 nd 200 WM in the cse of the inctive FA. With 100 nmol FA dded, this is numericlly equl to % of FA molecules prtitioning in lipid bilyer. In cse of the inctive FA the extent is not relted to prtitioning. b Incresed H lek. c Mesured with 10 WM, seprtely clibrted nd ccounted for shift due to bsorbnce. d Clculted with regrds to extent of H relese for luric cid. hlf protonted molecules t ph 7.2 in the cse of dicrboxylic cids tht could mimic the monovlent lurte (myristte) nions. The negligible cidi ction suggested the second protonted crboxyl group represents entity so polr it prevents the ip- op. The less polr bromo group ws tolerted since 12-bromododecnoic cid ips rpidly (Tble 1). All 2-hydroxy-FA tested were ctive. With exception of 2- hydroxyluric cid, ll 2-hydroxy-FA exhibited fster rtes nd higher extent of H relese thn their bsic nlogs (Tble 1). The 2-hydroxymyristic cid ws the fstest studied with 3-hydroxymyristic cid only slightly slower. Steric cid exhibited low extent of H relese with t12 of 2.5 s. Interestingly, 12-hydroxysteric cid ws found lso to be ctive nd fstest mong sterte series (Fig. 1, Tble 1). One cn explin it by shielding e ect of the til hexyl chin on the hydroxy group. Such shielding elimintes the originl bipolr chrcter of the hydroxylted C12-liphtic chin. Also bipolr 16-hydroxyplmitic cid exhibited fst cidi ction of moderte extent (Tble 1), thus behving distinctly from the shorter `til'-substituted FA. Hexdecnedioic cid induced Tble 2 Prtitioning of the selected ftty cids into the lipid bilyer s evluted using ADIFAB Ftty cid Binding to ADIFAB K d (WM) Prtition coe cient K Oleic cid Myristic cid Luric cid Tetrdecnedioic cid Hydroxyluric cid Hydroxymyristic cid Hydroxyluric cid in nite Binding of FA to ADIFAB ws mesured in the bsence nd presence of liposomes (18 WM) formed from L-K-phosphtidylcholine, crdiolipin nd 1% L-K-phosphtidic cid nd the corresponding K d vlues nd prtition coe cients were clculted s described in Section 2. 2-Hydroxy-luric cid did not bind to ADIFAB nd ddition of liposomes did not chnge the ADIFAB uorescence t ny 2-hydroxy-luric cid concentrtion. This provides evidence tht liposomes per se re not ecting ADIFAB. p
5 Acknowledgements : P. Jezí ek et l./febs Letters 408 (1997) 161^ smll drop in the ph in (Tble 1), but it did induce high H lek so we cnnot exclude the lytic chrcter of the e ect. We further scribed 9,10,16-trihydroxyplmitic cid (leuritic cid) s inctive (Fig. 1 nd Tble 1), becuse it cused negligible cidi ction, with n estimted t12 over 4 min. The derivtives bering benzene ring, i.e. phenylvleric nd phenylhexnoic cids nd derivtives with two benzene rings such s biphenylcrboxylic cid, 3,3-diphenylpropionic cid nd L-npthtoic cid re inctive (Fig. 1 nd Tble 1). The phenyl group with lesser polrity thn the hydroxy-group probbly prevents the trnsmembrne ip- op due to bulkiness nd plnr structure of the benzene ring. It is benzene ring t the til which is not tolerted, since dodecyloxy-benzoic nd heptylbenzoic cids re ctive. The ltter is very potent nd belongs to the fstest FA studied (Fig. 1 nd Tble 1). FA bering bulky but overll less polr groups such s 12- TNP-luric, 12-(4-zido-2-nitrophenyl) minododecnoic [17], 12-DOXYL- nd 5-DOXYL-steric cids [7,18] were found to ip- op with fst rte. The rst two re nother exmples of shielding e ect. The NO 2 group substitutions on the romtic ring convert it to n entity tolerted by ip- op. Inbility of FA to exert fst ip- op is very importnt property. The trivil explntion for lck of ip- op is the lck of prtitioning of the inctive FA into the lipid bilyer. We hve, however, observed otherwise. Using HPLC detection we showed tht 15.5% of 12-hydroxyluric cid is retined in the liposomes fter their pssge through the Sephdex G column, s compred to 27.8% of luric cid. Also Fig. 3 demonstrtes the prtitioning of 12-hydroxyluric nd tetrdecnedioic cids into liposomes (Fig. 3d,b) s compred to their ctive counterprts, oleic nd luric cid (Fig. 3,c). In ll cses, including the 12-hydroxyluric nd tetrdecnedioic cids, it is shown tht the equilibrium between ADI- FAB nd queous phse is strongly disturbed by the presence of liposomes (20 WM lipid concentrtion). Prtitioning into lipids is lso implied from clcultions of the respective prtition coe cients K p (Tble 2). The evluted K d vlues for FA binding to ADIFAB (Tble 2) were not directly relted to the FA bility to ip- op. For exmple, the binding of K- or L-hydroxy-FA to ADIFAB ws very poor. At present we re unwre of physicochemicl mechnism which prevents some FA derivtives from rpid ip- op cross the lipid bilyer. Considering tht even pyrenenonnoic cid exhibited ip- op with t s [7], inbility of some bipolr FA to ip- op in the time scle of minutes is surprising. The only FA previously reported to exhibit slow ip- op ws 12-(9-nthroyloxy)-steric cid (t12 of 200 s). A rther trivil explntion for the inbility of ip- op would be tht prtitioning of the inctive FA into the lipid phse is very low. We excluded this possibility by showing tht the inctive FA do prtition into the lipid bilyer, s detected from their interctions with ADIFAB. Therefore, we suggest tht rther speci c conformtion of the inctive FA in the membrne is the cuse for lck of rpid ip- op. Perhps U- shpe conformtion in the cse of bipolr FA or `dumbbell' shpe of the `til'-phenyl-substituted FA. The properties of the inctive FA with regrd to the lipid bilyer deserve further studies by physicochemicl methods. We lso strongly recommend to use the inctive FA s controls for studying the FAinduced phenomen such s uncoupling, ctivtion of proteins, etc. This work hs been supported by the grnt of the US-Czechoslovk Science nd Technology Progrm No ; by the Grnt No. 301/95/0620 of the Grnt Agency of the Czech Republic (to P.J.) nd by NIH Grnt GM31086 (to K.D.G). HPLC work ws provided by Dr. I. Miksí èk, Dept. of Anlysis of Biologiclly Active Substnces, Institute of Physiology, Prgue. References [1] D.W. Demer, J.W. Nichols, J Membr Biol 107 (1989) 91^103. [2] G. Krishnmoorthy, P.C. Hinkle, Biochemistry 23 (1984) 1640^ [3] M.P. Murphy, Biochim Biophys Act 977 (1989) 123^141. [4] H.-J. Freisleben, K. Zwicker, P. Jezíek, G. John, A. Bettin-Bogutzki, K. Ring, T. Nwroth, Chem Phys Lipids 78 (1995) 137^ 147. [5] J. Gutknecht, Proc Ntl Acd Sci USA 84 (1987) 6443^6446. [6] F. Kmp, J.A. Hmilton, Proc Ntl Acd Sci USA 89 (1992) 11367^ [7] F. Kmp, J.A. Hmilton, Biochemistry 32 (1993) 11074^ [8] L. Wojtczk, P. Schoënfeld, Biochim Biophys Act 1183 (1993) 41^57. [9] V.P. Skulchev, FEBS Lett 294 (1991) 158^162. [10] K.E. Grlid, D.E. Orosz, M. Modrinskyè, S. Vssnelli, P. Jezíek, J Biol Chem 271 (1996) 2615^2620. [11] D.E. Orosz, K.D. Grlid, Anl Biochem 210 (1993) 1^15. [12] T. Hnisí, M. Smrzí, P. Kl èr, K. Mcek, J. Kl èm, J. Bse, Z. Deyl, J Chromtog 452 (1988) 443^457. [13] M. Lngner, T. Isc, S.W. Hui, Biochim Biophys Act 1236 (1995) 73^80. [14] A. Anel, G.V. Richieri, A.M. Kleinfeld, Biochemistry 32 (1993) 530^536. [15] G.V. Richieri, R.T. Ogt, A.M. Kleinfeld, J Biol Chem 267 (1992) 23495^ [16] K.D. Grlid, A.D. Bevis, S.K. Rtkje, Biochim Biophys Act 976 (1989) 109^120. [17] P. Jezíek, J. Hnusí, C. Semrd, K.D. Grlid, J Biol Chem 271 (1996) 6199^6205. [18] P. Jezíek, H.-J. Freisleben, FEBS Lett 343 (1994) 22^26.
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