Pro- and anti-oxidant activities of the mitochondrial respiratory chain: factors influencing NAD P H-induced lipid peroxidation
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1 Ž. Biochimic et Biophysic Act Pro- nd nti-oxidnt ctivities of the mitochondril respirtory chin: ž / fctors influencing NAD P H-induced lipid peroxidtion M.A. Glinn,1, C.P. Lee,), L. Ernster Deprtment of Biochemistry, Wyne Stte UniÕersity School of Medicine, 540 E. Cnfield Street, Detroit, MI 48201, USA Deprtment of Biochemistry, Arrhenius Lortories, Stockholm UniÕersity, S Stockholm, Sweden Received 16 August 1996; revised 9 Octoer 1996; ccepted 14 Octoer 1996 Astrct This pper is study of fctors influencing the rte of lipid peroxidtion in eef hert sumitochondril prticles induced y NADŽ P. H vi the NADH-uiquinone oxidoreductse Ž Complex I. of the respirtory chin. In ccordnce with erlier oservtions, oth NADH nd NADPH initited lipid peroxidtion in the presence of ADP-Fe. The rte of the rection, mesured s oxygen consumption nd formtion of thiorituric cid rective sustnces, ws iphsic s function of NADH concentrtion, reching mximum t low NADH concentrtions nd then declining. In contrst, the NADPH-initited lipid peroxidtion showed monophsic concentrtion profile of hyperolic chrcter. Rotenone did not eliminte the iphsicity of the NADH-induced rection, indicting tht this ws not due to n ntioxidnt effect of reduced uiquinone t high NADH concentrtions. This conclusion ws further supported y the demonstrtion tht extrction of uiquinone from the prticles did not relieve the inhiition of lipid peroxidtion y high NADH concentrtions. However rhein, nother inhiitor of Complex I, eliminted the iphsicity, nd even cused sustntil stimultion of the NADH-induced lipid peroxidtion in the prticles upon extrction of uiquinone y pentne. No similr effect occurred in the cse of NADPH-induced lipid peroxidtion. Furthermore, rhein fcilitted oth NADH- nd NADPH-induced lipid peroxidtion even in the sence of dded ADP-Fe, in fshion similr to tht erlier reported with succinte in the presence of theonyltrifluorocetone. Bsed on these findings nd mesurements of the redox sttes of uiquinone nd cytochromes in the presence of KCN nd NADH or NADPH, it is concluded tht Complex I my distinguish etween electron input from NADH nd NADPH y differences in the sitež. s of sustrte inding nd in the pthwys nd rtes of NADH nd NADPH oxidtion. Ž. Keywords: Sumitochondril prticle; Lipid peroxidtion; Uiquinone; Rhein; Bovine hert Arevitions: SMP, sumitochondril prticles; UQ, uiquinone; TBARS, thiorituric cid rective sustnces; TTFA, theonyl trifluorocetone; EFA, ethoxyformic cid; UHDBT, 5-n-undecyl-6-hydroxy-4,7-dioxoenzothizol; PQQ, pyrrol quinoline quinone. ) Corresponding uthor. Fx: q1 Ž ; E-mil: cplee@med.wyne.edu 1 Present ddress: Lilly Reserch Lortories, Lilly Corporte Center, Indinpolis, IN 46285, USA. 1. Introduction Enzymic initition of lipid peroxidtion in eef hert sumitochondril prticles Ž SMP. occurs during the oxidtion of NADH or NADPH in the presence of suitle iron chelte w1 6 x. Elucidtion of the rection mechnism therefore requires identifiction of the NADŽ P. H-linked ctlyst involved in this process. The most commonly proposed ctlyst is the NADH-uiquinone Ž UQ. oxidoreductse Ž Complex I r97r$17.00 Copyright q 1997 Elsevier Science B.V. All rights reserved. Ž. PII S
2 M.A. Glinn et l.rbiochimic et Biophysic Act of the respirtory chin w2,3,5 x. However, while the oxidtion of NADH y Complex I hs een extensively studied, the oxidtion of NADPH y the sme complex is not well understood Žcf. reviews in referw7 9 x.. For numer of yers it hs een ences shown tht eef hert sumitochondril prticles consume NADPH t ph- 7, in rotenone-sensitive mnner, ut t much lower rte nd with higher K thn those found for NADH w10,11 x m. EPR studies hve demonstrted tht NADPH incompletely reduces the iron sulfur centers of Complex I s comw11 15 x. On this sis, it hs een pred with NADH suggested tht the NADPH-inding site is distinct from tht for NADH w10,11 x. Alrcht nd co-workers hve proposed model for the eef hert Complex I in which the enzyme is heterodimer with different complements of iron sulfur clusters, ech of which contins nicotinmide nucleotide-inding site, ut only one of which inds NADPH w13 15 x. It hs een shown y Tkeshige et l. w1 4x tht NADH nd NADPH cn initite lipid peroxidtion in eef hert SMP in the presence of ADP nd Fe. The process, followed y mesurement of oxygen consumption nd of the formtion of thiorituric cid rective sustnces Ž TBARS., ws found to e iphsic s function of the NADH concentrtion, reching mximl rte t low concentrtion of NADH. In contrst, the NADPH-initited lipid peroxidtion reveled monophsic concentrtion profile of hyperolic chrcter, reching mximl rte similr to tht otined t low NADH concentrtions. These oservtions were interpreted in terms of difference etween the ilities of NADH nd NADPH to reduce UQ vi the NADH-UQ oxidoreductse Ž Complex I. of the respirtory chin, i.e., to estlish n dequte stedy stte concentrtion of reduced UQ Ž uiquinol., the ltter cting s n ntioxidnt. An inhiition of lipid peroxidtion ws lso shown to occur upon the ddition of succinte, which reduced UQ vi succinte-uq oxidoreductse ŽCom- plex II.. When UQ ws extrcted from the prticles y pentne, the inhiition of lipid peroxidtion y succinte ws olished, nd could e restored y reincorportion of UQ into the prticles. The role of uiquinol s iologicl ntioxidnt hs in recent yers extensively een studied in numer of lortories Žsee refs. w16 18 x.. In previous pper wx 5 we hve confirmed the ove findings of Tkeshige et l. w1 4 x. However, we found tht the iphsic profile of the rte of lipid peroxidtion s function of the NADH concentrtion lso occurs in the presence of rotenone, which inhiits the reduction of UQ vi Complex I. Our results indicted tht fctorž. s other thn UQ my e involved in the iphsic response of the ADP-Fe - medited lipid peroxidtion system to incresing NADH concentrtion, nd tht these fctors, lthough locted efore the rotenone-sensitive site of Complex I, do not respond to NADPH. The purpose of the present work ws to chrcterize these fctors, which my e of interest for understnding the pro- nd nti-oxidnt ctivities of the mitochondril respirtory chin in controlling lipid peroxidtion. Prts of this work hve een communicted riefly w19,20 x. 2. Mterils nd methods Beef hert sumitochondril prticles Ž SMP. were prepred s descried y Lee w21 x, except tht EDTA ws omitted from the soniction medium nd 100 mg cytochrome crmg mitochondril protein ws dded to the mitochondril suspension efore ph djustment nd sonic disintegrtion. UQ-depleted nd UQ-replenished SMP were prew22x s modified y Ernster et l. w23 x. As the extrction pred ccording to the methods of Szrkowsk nd replenishment procedures require lyophilized prticles, control SMP were lso lyophilized efore resuspension in the incution medi. Ntive prticles were used s controls in studies not requiring UQ-depleted or UQ-replenished SMP. Lipid peroxidtion ws initited y the ddition of ADP-Fe nd NADH or NADPH. The detiled experimentl conditions re descried in the Tle nd Figure legends. Oxygen consumption ws mesured polrogrphiclly t 308C with Clrk-type oxygen electrode in 1 ml cpcity chmer. Oxygen uptke ws recorded for 10 min unless otherwise indicted. Susequently, 0.5 ml of the rection mixture ws removed from the oxygrph chmer, nd the enzyme rection ws terminted y the ddition of 0.5 ml of 30% trichlorocetic cid. TBARS were then determined s mesure of the extent of lipid peroxidtion y the thiorituric cid colorimetric test w24 x.
3 248 M.A. Glinn et l.rbiochimic et Biophysic Act Cytochrome contents were determined from reduced minus oxidized difference spectr recorded t room temperture, s descried previously w5,25x using n Aminco DW2000 split emrdul wvelength spectrophotometer in the split em mode. Amounts of cytochromes reducile y NADŽ P. H were relted to those reducile y dithionite, tking the ltter s 100%. Extents of reduction of UQ were determined fter incution of SMP with 1 mm KCN nd either NADH Ž s., NADPH Ž 1 8 min., or KBH 4 Ž 1 2 min., in deoxygented medi under nitrogen strem, t 258C in 1 ml cuvette. Protection of the smple from the ir during the incution procedure ws criticl for the success of the ssy. UQ ws then extrcted, nd reduced nd oxidized frctions were determined y HPLC coupled to UV nd electrow26 x. chemicl detection, s descried y Lee et l. Ž. Fig. 1. Effect of rhein on NAD P H-dependent lipid peroxidtion in SMP in the presence nd sence of ADP-Fe mesured s Ž A. oxygen consumption nd Ž B. TBARS formtion: The rection mixture consisted of 0.9 ml of 0.15 M KCl, 25 mm Tris-HCl Ž ph 6.5., 2.5 mm rotenone nd 1.0 mg SMP protein. Others s indicted were: 40 mm rhein, nd 1.0 mm ADPr10 mm Fe, nd vrying concentrtions of NADH Ž left. or NADPH Ž right.. Totl volume: 1.0 ml; temperture: 308C. Ž I,`. control SMP, Ž B,v. control SMPqrhein, Ž ^,^. UQ-depleted SMP, Ž ','. UQ-depleted SMPqrhein.
4 M.A. Glinn et l.rbiochimic et Biophysic Act Protein ws determined y the method of Lowry et l. w27x with ovine serum lumin s the stndrd. Horse hert cytochrome c ws otined from Sigm Ž St. Louis, MO.. All chemicls nd regents were of the purest grdes commercilly ville. Pentne ws distilled efore used for UQ extrction or replenishment. Glss-redistilled wter ws used throughout ll experiments. 3. Results 3.1. Effects of UQ depletion nd rhein on NAD P H- induced lipid peroxidtion Fig. 1 shows the effects of UQ depletion nd rhein on the lipid peroxidtion ctivity of SMP in the presence of rotenone, ADP-Fe, nd vrying concentrtions of NADH or NADPH. In the cse of NADH the concentrtion profile ws iphsic despite the presence of rotenone, in ccordnce with erlier oservtions wx 5. Removl of UQ from the prticles did not olish the iphsicity Ževen though the mximl ctivity ws somewht diminished., which further supports the contention tht the decrese in lipid peroxidtion ctivity upon incresing in the Tle 1 Effects of rhein on NADŽ P. H-dependent lipid peroxidtion in SMP in the sence nd presence of ADP-Fe Condition n nmol O2 nmol TBARS consumed produced NADH q rotenone no ddition " "0.1 qrhein " "0.2 3 qadp-fe " "0.9 qrheinqadp-fe " "0.6 NADPH q rotenone no ddition 5 0.0" "0.0 qrhein 5 6.2" "0.1 qadp-fe " "0.3 qrheinqadp-fe " "0.2 The rection mixture consisted of 0.9 ml of 0.15 M KClr25 mm Tris-HCl Ž ph 6.5., either 0.1 mm NADH or 0.2 mm NADPH, nd 1.0 mg SMP protein. Others when indicted: 2.5 mm rotenone, 50 mm rhein. Totl volume: 1.0 ml; temperture: 308C. Averge rtes re reported. Sttisticl difference from vlue for no ddition: P Tle 2 Effects of rhein on NADŽ P. H-dependent lipid peroxidtion in UQ-depleted SMP in the sence nd presence of ADP-Fe Condition n nmol O2 nmol TBARS consumed produced NADH q rotenone qadp-fe " "0.4 qrhein " "0.6 qrheinqadp-fe " "0.7 qrheinqedta "6.3 c 0.6"0.1 NADPH q rotenone qadp-fe " "0.3 qrhein 5 4.6" "0.1 qrheinqadp-fe " "0.3 qrheinqedta Experimentl conditions were s in Tle 1, except UQ-depleted SMP ws used. Sttisticl difference etween the presence nd sence of rhein: P Sttisticl difference etween the presence nd sence of 10 mm EDTA: P -0.01; c P Tle 3 NADH nd NADPH oxidse ctivities of SMP Condition ph n nmol O2 rmin per mg SMP protein NADH no inhiitor "270.6 no inhiitor "237.2 qrhein "58.1 qrotenone "0.0 qefa qntimycin "0.0 quhdbt "9.6 qmyxothizol "14.2 NADPH no inhiitor "0.0 no inhiitor "3.3 qrhein "4.9 qrotenone "2.2 qefa qntimycin "3.4 quhdbt "1.8 myxothizol "0.1 The rection mixture consisted of 0.9 ml medium, mm NADH or 0.4 mm NADPH, mgrml SMP protein ŽNADH oxidse. nd 1.0 mgrml SMP protein Ž NADPH oxidse.. Concentrtions of other dditions: 50 mm rhein, 2.5 mm rotenone, 0.6 mm EFA, 1 mm ntimycin, 10 mm UHDBT, 2 mm myxothizol. Totl volume: 1.0 ml; temperture: 308C. Mximl rtes re reported. Sttisticl differences from vlue with no inhiitor t ph 6.5: P -0.05, P
5 250 M.A. Glinn et l.rbiochimic et Biophysic Act NADH concentrtion ws not due to reduction of UQ. However, rhein Ž4,5-dihydroxynthrquinone-2- croxylic cid., competitive inhiitor of Complex I with respect to NADH w28 x, olished the iphsicity of the NADH concentrtion profile, nd in the UQ-depleted prticles it even cused 4- to 5-fold stimultion of lipid peroxidtion. In the cse of NADPH, depletion of UQ from the prticles resulted in decrese in lipid peroxidtion, nd rhein hd no significnt effect on either the control or the UQ-depleted prticles. Rhein induced n NADŽ P. H-dependent lipid peroxidtion even in the sence of ADP-Fe, oth in the control nd the UQ-depleted prticles ŽTles 1 nd 2., leit to lower extent thn tht found in the presence of ADP-Fe. This effect, which ws similr to tht erlier descried with succinte in the presence of theonyl trifluorocetone Ž TTFA. wx 5, ws inhiited y the iron cheltor EDTA Žcf. Tles 1 nd Comprison of NADH nd NADPH oxidse ctiõities To explore the sis for the difference etween the NADH- nd NADPH-induced lipid peroxidtion systems, vrious prmeters of the NADH nd NADPH oxidse ctivities of SMP were investigted. Tle 3 shows the respirtory rtes with NADH or NADPH s sustrtes. At ph 6.5, NADH induced rpid nd immedite oxygen uptke. The rection ws ctlyzed y the respirtory chin enzymes, s demonstrted y its sensitivity to the Complex I inhiitors rhein, rotenone nd ethoxyformic cid Ž EFA., nd y the inhiitors of uiquinol-cytochrome c oxidoreductse Ž Complex III. ntimycin, 5-n-undecyl-6-hydroxy-4,7-dioxoenzothizol Ž UHDBT. nd myxothizol. The uninhiited rte ws unchnged t ph 7.5. NADPH ws oxidized t - 2% of the rte for NADH t ph 6.5 nd to no detectle extent t ph 7.5 Ž Tle 3.. A lg phse of 2 4 min preceded the onset of oxygen uptke. The rection ws inhiited y rotenone nd myxothizol, showing tht it involved Complexes I nd III. Unlike the NADH oxidse, however, it ws only slightly inhiited y ntimycin, nd even stimulted y rhein Redox stte of cytochromes Tle 4 summrizes dt on the stedy stte levels of reduced cytochromes, c nd in SMP incuted Tle 4 Extent of reduction of cytochromes y NADŽ P. H in the presence of respirtory inhiitors Condition Cytochrome reduction Ž % of dithionite-reducile. c NADH control 60.9" " " 8.9 qrotenone 15.3" " " 26.2 qntimycin 76.7" " " 4.4 quhdbt 50.6" " " 14.0 qmyxothizol 82.9" " " 9.7 NADPH control 37.4" " " 14.4 qrotenone 1.1" " " 10.9 qntimycin 62.1" " " 21.1 quhdbt 14.0" " " 4.6 qmyxothizol 50.0" " " 18.8 Ž. The rection mixture consisted of 0.9 ml of 0.15 M KClr2 mm Mops ph 6.5, 1 mm KCN, 0.3 mm NADH nd 1.0 mgrml SMP protein. Concentrtions of other dditions: 2.5 mm rotenone, 2 mm ntimycin, 2 mm myxothizol, nd 10 mm UHDBT.
6 M.A. Glinn et l.rbiochimic et Biophysic Act in the presence of KCN nd NADH or NADPH, nd the chnges in these levels upon the susequent ddition of inhiitors of Complexes I or III. The vlues re expressed s percent of dithionite-reducile cytochromes. In the presence of KCN lone, the stedy stte levels of reduced cytochromes c nd were pproximtely equl in the presence of NADH nd NADPH, pprox. 80% nd 100%, respectively. The level of reduced cytochrome ws significntly lower in the cse of NADPH thn tht of NADH, pprox. 37% vs. 61%. It ws lso found tht NADPH reduced cytochromes c nd much more rpidly thn cytochrome Ž50 70 s pre-stedy stte lg for cytochromes c nd, vs. 460 seconds for ; with NADH, s for ll cytochromes; dt not shown.. Among the inhiitors tested, rotenone shrply decresed the mount of cytochrome reducile y oth nicotinmide nucleotides, ut hd much less effect with respect to cytochromes c nd. Antimycin, in contrst, incresed the mount of cytochrome reducile y oth NADH nd NADPH, in greement with its proposed site of ction on the Q cycle w29 x. Myxothizol lso incresed, wheres UHDBT decresed, the mount of cytochrome reducile y oth nicotinmide nucleotides. These findings suggested tht the difference in the interction etween Complex I s reduced y NADH or NADPH nd Complex III is primrily of kinetic nture nd my e governed y the redox stte of UQ Redox stte of UQ Support for the ove contention ws otined y mesuring the stedy stte level of UQ in SMP incuted with NADH or NADPH in the present of KCN Ž Tle 5.. After ddition of sturting concentrtions of NADH Ž mm. out 45% of the totl UQ ws reduced, which ws out one-hlf of the mount reducile y KBH 4. At the sme concentrtion of NADPH, there ws no detectle mount of reduced UQ. However, when the concentrtion of NADH ws decresed to non-sturting levels Ž9 15 mm., the mount of reduced UQ decresed to out 14%. Likewise, there ws decrese even t sturting NADH concentrtion in the presence of rhein, i.e., under conditions of limited electron input from NADH. As expected, rotenone inhiited UQ reduc- Tle 5 Reduction of UQ y NADŽ P. H Reductnt n nmol UQrmg % UQ reduced protein NADPH mm 6 4.4" "0.0 NADH 9 15 mm " " mm 2 3.7" " mm " " mmqrhein 2 3.9" "2.0 KBH " "3.4 None Experimentl conditions for SMP incution, UQ extrction nd quntittion were s descried in Section 2. The rection mixture consisted of nitrogented 0.15 M KClr2 mm Mops uffer ŽpH 6.5., 1 mm KCN, vrying concentrtions of NADŽ P. H or KBH 4 nd mgrml SMP protein. The concentrtion of rhein ws 50 mm. Sttisticl differences from vlue for 0.3 mm NADH: P P Sttisticl differences from vlue for 0.3 mm NADPH: c P -0.01, d P tion y NADH completely Ž dt not shown.. It is conceivle, therefore, tht the lck of reduction of UQ in the cse of NADPH my e due to the very slow electron input even t sturting NADPH concentrtion. Any electrons trnsferred to UQ my e lost through utoxidtion Effect of UQ depletion Dt summrized in Tle 6 compre the effects of UQ extrction nd reincorportion on the NADH nd NADPH oxidse ctivities of SMP. In ccordnce with erlier reports w22,23x extrction of UQ cused n inhiition of )95% of the NADH oxidse ctivity s compred to lyophilized controls. In contrst, NADPH-supported oxygen uptke ws not diminished upon removl of the ulk of UQ through pentne extrction. One possiility for the lck of effect of UQ extrction is gin the low rte of NADPH oxidtion in the control, which did not exceed tht found with NADH fter the pentne tretment. However, the lg time efore ttinment of mximl rte of oxygen uptke ws much longer Ž )5 min. when NADPH rther thn NADH ws the sustrte, regrdless of the presence of UQ; this ws true even when the mximl rtes otined with the d,c
7 252 M.A. Glinn et l.rbiochimic et Biophysic Act Tle 6 Oxygen uptke induced y respirtory sustrtes in lyophilized control, UQ-depleted nd UQ-replenished SMP Condition n nmol O rmin lg Ž min. 2 per mg protein NADH control SMP " "0.1 UQ-depleted SMP 6 5.6" "0.2 UQ-replenished SMP " "0.2 NADPH Control SMP 5 5.1" "1.1 UQ-depleted SMP " "1.8 UQ-replenished SMP 4 3.1" "0.4 The rection mixture consisted of 0.9 ml of 0.15 M KClr2 mm Mops Ž ph 6.5., 50 mgrml cytochrome c nd mgrml SMP protein. Totl volume: 1.0 ml; temperture: 308C. Mximl rtes re reported. Sttisticl differences from vlues for control SMP: P -0.01, P two nicotinmide nucletides were similr, s ws the cse with the UQ depleted SMP. The reson for this lg, which ws similr to tht found for the ttinment of stedy stte level of cytochrome reduction y NADPH in the presence of KCN Ž see ove., is uncler. However, it suggests tht there is difference etween the mechnisms y which the NADHnd NADPH-reduced Complex I intercts with UQ nd cytochrome. 4. Discussion The results presented here revel some novel spects of the role of Complex I of the mitochondril respirtory chin in oth promoting nd preventing lipid peroxidtion, i.e., in cting oth s pro- nd n nti-oxidnt, depending on the previling conditions. At low concentrtions of NADH nd in the presence of ADP-Fe, lipid peroxidtion proceeds t mximl rte, which decreses upon incresing the NADH concentrtion. This ltter effect, s lredy pointed out, cnnot e due to n inhiition of lipid peroxidtion y uiquinol, since it is lso oserved in the presence of rotenone, which inhiits UQ reduction. The present finding Ž Fig. 1. tht nother inhiitor of Complex I, rhein, olishes this inhiition, indictes tht the decline of the rte of lipid peroxidtion t high concentrtion is cused y componentž. s of Complex I locted etween the rhein- nd rotenonesensitive sites. It hs een reported tht pyrrolquinoline quinone Ž PQQ. occurs in mitochondri, serving s n electron crrier in Complex I t or ner the rotenone-sensitive site w30,31 x, nd tht in its reduced form it my ct s n ntoxidnt w32 x. Alterntively, it my e tht rhein, which is quinone, my e reduced y the flvoprotein component of Complex I nd give rise to redox cycling through the semiquinone, with the formtion of the superoxide rdicl nd the initition of lipid peroxidtion. Autoxidtion of uisemiquinone to UQ nd superoxide induces TBARS formtion t the S-3 iron sulfur center of Complex II in the presence of thenoyltrifluorocetone Ž TTFA. nd succinte wx 5. This redox cycling nd susequent lipid peroxidtion re prew33 x. In vented if 50% of the UQ in SMP ws reduced the cse of Complex I, such n initition my occur vi the nonheme iron component of Complex I djcent to the flvoprotein nd would thus explin the findings tht NADHq rhein cn initite lipid peroxidtion in the sence of ADP-Fe nd tht this process is inhiited y EDTA Ž Tle 2.. Reduced rhein my lso cuse non-enzymic reduction of UQ, nd would thus explin the very mrked increse in the rte of NADH nd ADP-Fe -induced lipid peroxidtion cused y rhein upon the extrction of UQ from the prticles Ž Fig. 1.. Furthermore, it hs een shown w34,35x tht extrction of SMP with pentne lso removes vitmin E, potent inhiitor of lipid peroxidtion which my e regenerted y uiquinol w36x nd proly lso y reduced rhein. These possiilities my e explored in the future y using isolted Complex I. Concerning the differences in properties etween the NADH- nd NADPH-induced lipid peroxidtion systems, these my e explined on the sis of the heterodimeric model of Complex I proposed y Alw13 15 x. According to this rcht nd ssocites model Žcf. ref. w15 x., the NADPH-rective monomer lcks one of the iron sulfur centers nd cn interct with UQ nd therey with Complex III only y trnsferring electron to the distl iron sulfur centers of the other monomer, rection tht is reltively slow nd requires n cidic ph. Interestingly, similr requirement for cidic ph hs erlier een reported for the interction of NADPH with lctte dehydrogense nd lcohol dehydrogense w37 x, sug-
8 M.A. Glinn et l.rbiochimic et Biophysic Act gesting tht the negtive chrge of the 3-phosphte group of NADPH is responsile for the virtul lck of rectivity of these enzymes with NADPH t ph 7.5. The sme considertion my pply for the interction of NADPH with Complex I. In ny cse, the model of Alrcht nd ssocites w13 15x my explin the present findings tht the reduction of UQ nd cytochrome is the rte-limiting step in NADPH oxidse. The lck of detectle reduction of UQ Ž Tle 5. nd the low stedy stte level of reduced cytochrome found with NADPH in the presence of KCN Ž Tle 4. re consistent with this conclusion. The reson for the long lg phse involved in the reduction of cytochrome is not cler, ut my e relted to ck-flow of electrons from cytochrome to UQ vi the Q cycle; notly, no similr lg is found when NADH is oxidized t the sme low rte s NADPH Ž cf. Tle 6.. The increse in cytochrome reduction occurring upon the ddition of ntimycin to the KCN-supplemented system my e due to the inhiition of this ck-flow. In fct, similr phenomenon hs een oserved with succinte or NADH s sustrte in UQ-depleted prticles w23x or in prticles in which the ulk of UQ hs een destroyed through lipid peroxidtion w38 x. In this connection, it is of interest to refer to erlier conclusions y Rossi et l. w39x nd y Dooijewrd nd Slter w40x tht UQ cts s feedck regultor of succinte dehydrogense nd NADH dehydrogense, respectively, sed on experiments with UQ-depleted preprtions. The common denomintor in ll of these systems is the very low rte of electron input from the sustrtes, NADPH, NADH or succinte, into Complex III. However, wheres the exmples of the UQ-deficient systems represent rtificil conditions, the NADPH oxidse ctivity ppers to e ntive feture of the mitochondril respirtory chin, the iochemicl nd physiologicl functions of which deserve continued investigtion. Acknowledgements This work hs een supported y grnts from the Ntionl Institutes of Helth, USA Ž CPL. nd the Swedish Nturl Science Reserch Council Ž LE.. We thnk Mrs. Sue Hr Tsng for her skillful technicl ssistnce. References wx 1 Tkeshige, K. nd Minkmi, S. Ž J. Biochem. Ž Jpn. 77, wx 2 Tkyngi, R., Tkeshige, K. nd Minkmi, S. Ž Biochem. J. 192, wx 3 Tkeshige, K., Tkyngi, R. nd Minkmi, S. Ž Biochem. J. 192, wx 4 Nryshi, H., Tkeshige, K. nd Minkmi, S. Ž Biochem. J. 202, wx 5 Glinn, M., Ernster, L. nd Lee, C.P. Ž Arch. Biochem. Biophys. 290, wx 6 Ernster, L. Ž in Active Oxygen nd Antioxidnts ŽYgi, K., ed.., pp. 1 38, CRC Press, Boc Rton, FL. wx 7 Singer, T.P. nd Rmsy, R.R. Ž in Moleculr Mechnisms in Bioenergetics Ž Ernster, L., ed.., pp , Elsevier, New York. wx 8 Wlker, J.E. Ž Q. Rev. Biophys. 25, wx 9 Rgn, C.I. Ž in Current Topics in Bioenergetics ŽLee, C.P., ed.., Vol. 15, pp. 1 36, Acdemic Press, New York. w10x Htefi, Y. Ž Biochem. Biophys. Res. Commun. 50, w11x Htefi, Y. nd Hnstein, W.G. Ž Biochemistry 12, w12x Htefi, Y. nd Berden, A.J. Ž Biochem. Biophys. Res. Commun. 69, w13x Bkker, P.T.A. nd Alrcht, S.P.J. Ž Biochim. Biophys. Act 850, w14x Alrcht, S.P.J. nd Bkker, P.T.A. Ž Biochim. Biophys. Act 850, w15x Vn Belzen, R. nd Alrcht, S.P.J. Ž Biochim. Biophys. Act 974, w16x Beyer, R.E. nd Ernster, L. Ž in Highlights in Uiquinone Reserch ŽLenz, G., Brnei, O., Ri, A., Bttino, M., eds.., pp , Tylor nd Frncis, London. w17x Ernster, L. Ž in Oxidtive Processes nd Antioxidnts ŽPoletti, R., Smuelsson, B., Ctpno, A.L., Poli, A. nd Rinetti, M., eds.., pp , Rven Press, New York. w18x Ernster, L. nd Dllner, G. Ž Biochim. Biophys. Act 1271, w19x Glinn, M., Ernster, L. nd Lee, C.P. Ž FASEB J. 6, w20x Glinn, M., Ernster, L. nd Lee, C.P. Ž Biophys. J. 64, A103. w21x Lee, C.P. Ž Methods Enzymol. 55, w22x Szrkowsk, L. Ž Arch. Biochem. Biophys. 113, w23x Ernster, L., Lee, I.Y., Norling, B. nd Persson, B. Ž Eur. J. Biochem. 9, w24x Bernheim, F., Bernheim, M. nd Wilur, K. Ž J. Biol. Chem. 174, w25x Lee, C.P., Ernster, L. nd Chnce, B. Ž Eur. J. Biochem. 8, w26x Lee, C.P., Mrtens, M.E. nd Tsng, S. Ž Methods Toxicol. 2,
9 254 M.A. Glinn et l.rbiochimic et Biophysic Act w27x Lowry, L.H., Rosenrough, N.J., Frr, A.L. nd Rndll, R.J. Ž J. Biol. Chem. 193, w28x Singer, T.P. Ž Methods Enzymol. 55, w29x Trumpower, B.T. Ž J. Biol. Chem. 265, w30x Mh, J., Pz, M.A., Fluckiger, H. nd Gllop, P.M. Ž FASEB J. 7, A53. w31x Mh, J., Pz, M.A., Fluckiger, R., Lrdy, H. nd Gllop, P.M. Ž Astrct 58, Society of Toxicology Annul Meeting. w32x Gllop, P.M., Pz, M.A., Fluckiger, R. nd Benson, E. Ž Connect. Tissue Res. 29, w33x Eto, Y., Kng, D., Hsegw, E., Tkeshige, K. nd Minkmi, S. Ž Arch. Biochem. Biophys. 295, w34x Forsmrk, P., Aerg, F., Norling, B., Nordenrnd, K., Dllner, G. nd Ernster, L. Ž FEBS Lett. 285, w35x Ernster, L., Forsmrk, P. nd Nordenrnd, K. Ž Biofctors 3, w36x Kgn, V., Serinov, E. nd Pcker, L. Ž Biochem. Biophys. Res. Commun. 169, w37x Nvzio, F., Ernster, B.B. nd Ernster, L. Ž Biochim. Biophys. Act 26, w38x Forsmrk-Andree, P, Lee, C.-P, Dllner, G. nd Ernster, L. Ž Free Rdic. Biol. Med. 22, w39x Rossi, E., Norling, B., Persson, B. nd Ernster, L. Ž Eur. J. Biochem. 16, w40x Dooijewrd, G. nd Slter, E.C. Ž Biochim. Biophys. Act 440, 1 15.
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