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• W2015761041 abstract "All members of the Oxa1/Alb3/YidC family have been implicated in the biogenesis of respiratory and energy transducing proteins. In Escherichia coli, YidC functions together with and independently of the Sec system. Although the range of proteins shown to be dependent on YidC continues to increase, the exact role of YidC in insertion remains enigmatic. Here we show that YidC is essential for the insertion of subunit K of the NADH:ubiquinone oxidoreductase and that the dependence is due to the presence of two conserved glutamate residues in the transmembrane segments of subunit K. The results suggest a model in which YidC serves as a membrane chaperone for the insertion of the less hydrophobic, negatively charged transmembrane segments of NuoK. All members of the Oxa1/Alb3/YidC family have been implicated in the biogenesis of respiratory and energy transducing proteins. In Escherichia coli, YidC functions together with and independently of the Sec system. Although the range of proteins shown to be dependent on YidC continues to increase, the exact role of YidC in insertion remains enigmatic. Here we show that YidC is essential for the insertion of subunit K of the NADH:ubiquinone oxidoreductase and that the dependence is due to the presence of two conserved glutamate residues in the transmembrane segments of subunit K. The results suggest a model in which YidC serves as a membrane chaperone for the insertion of the less hydrophobic, negatively charged transmembrane segments of NuoK. IntroductionIn Escherichia coli the inner membrane contains essential energy transducing complexes such as components of the electron transport chain. The majority of inner membrane proteins are inserted cotranslationally via the general secretory pathway otherwise known as the Sec system. In this pathway, the bacterial signal recognition particle targets ribosome-bound nascent chains to the SecYEG translocase via the signal recognition particle receptor FtsY. Membrane insertion of these proteins proceeds by a cotranslational “threading mechanism” in which the accessory protein YidC is postulated to play an important role in the clearance of transmembrane segments (TMSs) 2The abbreviations used are: TMStransmembrane segmentIMVinner membrane vesiclePMFproton motive forceNTAnitrilotriacetic acid. from the SecYEG channel (1Scotti P.A. Urbanus M.L. Brunner J. de Gier J.W. von Heijne G. van der Does C. Driessen A.J. Oudega B. Luirink J. EMBO J. 2000; 19: 542-549Crossref PubMed Scopus (299) Google Scholar, 2de Gier J.W. Luirink J. Mol. Microbiol. 2001; 40: 314-322Crossref PubMed Scopus (82) Google Scholar). A small subset of integral membrane proteins are targeted directly to YidC where they are integrated into the membrane in a Sec-independent manner. YidC belongs to the evolutionarily conserved Oxa1/Alb3/YidC family. Oxa-related proteins have been identified in all genomes sequenced to date and are postulated to have evolved before the divergence of the three major domains of life (3Pohlschröder M. Hartmann E. Hand N.J. Dilks K. Haddad A. Annu. Rev. Microbiol. 2005; 59: 91-111Crossref PubMed Scopus (97) Google Scholar, 4Yen M.R. Harley K.T. Tseng Y.H. Saier Jr., M.H. FEMS Microbiol. Lett. 2001; 204: 223-231Crossref PubMed Google Scholar, 5Luirink J. Samuelsson T. de Gier J.W. FEBS Lett. 2001; 501: 1-5Crossref PubMed Scopus (121) Google Scholar). Oxa1 (oxidase assembly) from yeast was the first member of this family to be described (6Bauer M. Behrens M. Esser K. Michaelis G. Pratje E. Mol. Gen. Genet. 1994; 245: 272-278Crossref PubMed Scopus (106) Google Scholar, 7Bonnefoy N. Chalvet F. Hamel P. Slonimski P.P. Dujardin G. J. Mol. Biol. 1994; 239: 201-212Crossref PubMed Scopus (179) Google Scholar). It was originally identified as an essential factor for the biogenesis of respiratory complexes in the mitochondrion, more specifically for the insertion of subunits of the cytochrome bc1 oxidase and ATP synthase (8Altamura N. Capitanio N. Bonnefoy N. Papa S. Dujardin G. FEBS Lett. 1996; 382: 111-115Crossref PubMed Scopus (124) Google Scholar). Alb3 is located in the thylakoid membranes of plant chloroplasts and involved in the biogenesis of light harvesting complexes (9Moore M. Harrison M.S. Peterson E.C. Henry R. J. Biol. Chem. 2000; 275: 1529-1532Abstract Full Text Full Text PDF PubMed Scopus (184) Google Scholar). In E. coli it has been shown that YidC is essential for the insertion of subunit c and a of the F1F0 ATP synthase (Foc and Foa) (10van der Laan M. Bechtluft P. Kol S. Nouwen N. Driessen A.J. J. Cell Biol. 2004; 165: 213-222Crossref PubMed Scopus (174) Google Scholar, 11Yi L. Jiang F. Chen M. Cain B. Bolhuis A. Dalbey R.E. Biochemistry. 2003; 42: 10537-10544Crossref PubMed Scopus (100) Google Scholar), subunit a of cytochrome o oxidase (CyoA) (12du Plessis D.J. Nouwen N. Driessen A.J. J. Biol. Chem. 2006; 281: 12248-12252Abstract Full Text Full Text PDF PubMed Scopus (71) Google Scholar, 13van Bloois E. Haan G.J. de Gier J.W. Oudega B. Luirink J. J. Biol. Chem. 2006; 281: 10002-10009Abstract Full Text Full Text PDF PubMed Scopus (64) Google Scholar), and MscL, the mechanosensitive channel of large conductance (14Facey S.J. Neugebauer S.A. Krauss S. Kuhn A. J. Mol. Biol. 2007; 365: 995-1004Crossref PubMed Scopus (90) Google Scholar).Although members of the family have all been implicated in membrane protein biogenesis of respiratory and energy transducing proteins, there is a great variance in substrate specificity within the family. For example Oxa1 proteins appear to have a varying role in the biogenesis of respiratory complexes I, III, IV, and V as illustrated by studies in Neurospora crassa, (15Nargang F.E. Preuss M. Neupert W. Herrmann J.M. J. Biol. Chem. 2002; 277: 12846-12853Abstract Full Text Full Text PDF PubMed Scopus (74) Google Scholar), Podospora anseria (16Sellem C.H. Lemaire C. Lorin S. Dujardin G. Sainsard-Chanet A. Genetics. 2005; 169: 1379-1389Crossref PubMed Scopus (26) Google Scholar), HEK293 cells (17Stiburek L. Fornuskova D. Wenchich L. Pejznochova M. Hansikova H. Zeman J. J. Mol. Biol. 2007; 374: 506-516Crossref PubMed Scopus (67) Google Scholar), and Saccharomyces cerevisiae (6Bauer M. Behrens M. Esser K. Michaelis G. Pratje E. Mol. Gen. Genet. 1994; 245: 272-278Crossref PubMed Scopus (106) Google Scholar, 7Bonnefoy N. Chalvet F. Hamel P. Slonimski P.P. Dujardin G. J. Mol. Biol. 1994; 239: 201-212Crossref PubMed Scopus (179) Google Scholar, 18Meyer W. Bauer M. Pratje E. Curr. Genet. 1997; 31: 401-407Crossref PubMed Scopus (22) Google Scholar, 19Lemaire C. Hamel P. Velours J. Dujardin G. J. Biol. Chem. 2000; 275: 23471-23475Abstract Full Text Full Text PDF PubMed Scopus (59) Google Scholar, 20Jia L. Dienhart M.K. Stuart R.A. Mol. Biol. Cell. 2007; 18: 1897-1908Crossref PubMed Scopus (79) Google Scholar). This highlights that although the general function of Oxa1/Alb3/YidC family proteins is known, each member plays a specific and in some cases yet to be identified role in the biogenesis of respiratory proteins.In a recent study, we showed that YidC depletion in E. coli resulted in a cessation of growth under anaerobic conditions and that this growth defect may be in part due to reduced levels of the complex I homolog in bacteria, the NADH:ubiquinone reductase, or NADH dehydrogenase I, in the membrane (21Price C.E. Driessen A.J. J. Biol. Chem. 2008; 283: 26921-26927Abstract Full Text Full Text PDF PubMed Scopus (27) Google Scholar). In particular, levels of the smallest membrane subunit K (NuoK) decreased. The aim of this study was to elucidate the role of YidC in NuoK membrane biogenesis and to determine the structural features of NuoK underlying this role. We found that in vitro synthesized NuoK requires both SecYEG and YidC for insertion and that two conserved negative charges in TMSs 2 and 3 determine the dependence of NuoK on YidC for insertion.DISCUSSIONAll of the subunits of the bacterial complex I, NADH dehydrogenase I, are encoded by the nuo operon. In E. coli, NADH dehydrogenase I contains 13 subunits, NuoA through to NuoN with NuoC and NuoD fused to form one protein. If any of these subunits are absent, a functional enzyme complex cannot be formed (37Schneider D. Pohl T. Walter J. Dörner K. Kohlstädt M. Berger A. Spehr V. Friedrich T. Biochim. Biophys. Acta. 2008; 1777: 735-739Crossref PubMed Scopus (40) Google Scholar). In a previous study, we showed that levels of the small membrane subunit NuoK are greatly reduced upon YidC depletion (21Price C.E. Driessen A.J. J. Biol. Chem. 2008; 283: 26921-26927Abstract Full Text Full Text PDF PubMed Scopus (27) Google Scholar). A decrease in the levels of NuoK in the membrane could have been due to the absence of one of the other subunits under YidC-depleting conditions, but as we now demonstrate, YidC is directly involved in the insertion of NuoK. Using IMVs we showed that the levels of YidC and SecYEG affected the efficiency of NuoK insertion. The decrease in insertion efficiency in YidC− IMVs was not due to the impaired ability of the IMVs to generate a PMF because in the absence of a PMF, the efficiency of insertion of NuoK was even enhanced. It has been shown with M13 procoat Lep and CyoA derivatives that the presence of positive charges in the translocated loops of these derivatives created proteins that only inserted in the absence of a PMF (38Samuelson J.C. Jiang F. Yi L. Chen M. de Gier J.W. Kuhn A. Dalbey R.E. J. Biol. Chem. 2001; 276: 34847-34852Abstract Full Text Full Text PDF PubMed Scopus (117) Google Scholar, 39Celebi N. Dalbey R.E. Yuan J. J. Mol. Biol. 2008; 375: 1282-1292Crossref PubMed Scopus (12) Google Scholar). NuoK contains one negatively charged residue in the periplasmic loop between TMSs 2 and 3, whereas the cytoplasmic loop between TMSs 1 and 2 and the C-terminal tail contain numerous positively charged amino acids. The protein topology therefore follows that predicted by the “positive inside rule” (40von Heijne G. Gavel Y. Eur. J. Biochem. 1988; 174: 671-678Crossref PubMed Scopus (566) Google Scholar), and it is not immediately obvious why the PMF would inhibit protein insertion. NADH dehydrogenase I is the preferred NADH dehydrogenase under anaerobic growth conditions (41Tran Q.H. Bongaerts J. Vlad D. Unden G. Eur. J. Biochem. 1997; 244: 155-160Crossref PubMed Scopus (111) Google Scholar). Unlike NADH dehydrogenase II, the proton-pumping NADH dehydrogenase I is energy-conserving, which is needed under the “energy limited” conditions of growth without oxygen. It is possible that NuoK insertion is enhanced under such conditions when the PMF is reduced and NADH dehydrogenase I is needed.Although the number of known YidC-dependent membrane proteins has increased during recent years, the exact mechanism of YidC in membrane protein insertion remains enigmatic. YidC has been shown to contact the TMSs of numerous integral membrane proteins in various cross-linking studies (24van der Laan M. Houben E.N. Nouwen N. Luirink J. Driessen A.J. EMBO Rep. 2001; 2: 519-523Crossref PubMed Scopus (95) Google Scholar, 42Yu Z. Koningstein G. Pop A. Luirink J. J. Biol. Chem. 2008; 283: 34635-34642Abstract Full Text Full Text PDF PubMed Scopus (35) Google Scholar, 43Beck K. Eisner G. Trescher D. Dalbey R.E. Brunner J. Müller M. EMBO Rep. 2001; 2: 709-714Crossref PubMed Scopus (136) Google Scholar), and yet YidC is dispensable in the insertion of most of these proteins (26van der Laan M. Nouwen N. Driessen A.J. J. Biol. Chem. 2004; 279: 1659-1664Abstract Full Text Full Text PDF PubMed Scopus (50) Google Scholar, 44Samuelson J.C. Chen M. Jiang F. Möller I. Wiedmann M. Kuhn A. Phillips G.J. Dalbey R.E. Nature. 2000; 406: 637-641Crossref PubMed Scopus (419) Google Scholar, 45van der Laan M. Urbanus M.L. Ten Hagen-Jongman C.M. Nouwen N. Oudega B. Harms N. Driessen A.J. Luirink J. Proc. Natl. Acad. Sci. U.S.A. 2003; 100: 5801-5806Crossref PubMed Scopus (125) Google Scholar). Using in vitro insertion into proteoliposomes, we show that NuoK minimally requires both YidC and SecYEG for insertion. Subunit a of the cytochrome oxidase, CyoA, has also been shown to require both YidC and SecYEG for insertion in vitro (12du Plessis D.J. Nouwen N. Driessen A.J. J. Biol. Chem. 2006; 281: 12248-12252Abstract Full Text Full Text PDF PubMed Scopus (71) Google Scholar). Based on the individual insertion requirements of constructs containing either the N- or C-terminal parts of CyoA, it has been suggested that SecYEG and YidC work sequentially in the insertion of CyoA with YidC inserting the N-terminal hairpin and SecYEG inserting the C-terminal TMS and long periplasmic C-terminal tail (13van Bloois E. Haan G.J. de Gier J.W. Oudega B. Luirink J. J. Biol. Chem. 2006; 281: 10002-10009Abstract Full Text Full Text PDF PubMed Scopus (64) Google Scholar, 46Celebi N. Yi L. Facey S.J. Kuhn A. Dalbey R.E. J. Mol. Biol. 2006; 357: 1428-1436Crossref PubMed Scopus (67) Google Scholar). This strict sequential insertion is only alleviated when a long linker between TMSs 1 and 2 is introduced, after which the C terminus can insert independently of the N-terminal hairpin (39Celebi N. Dalbey R.E. Yuan J. J. Mol. Biol. 2008; 375: 1282-1292Crossref PubMed Scopus (12) Google Scholar). Interestingly the introduction of numerous positive charges in the signal peptide and TMS 1 block the insertion of this protein via the YidC pathway but do not result in default insertion via the Sec translocon (39Celebi N. Dalbey R.E. Yuan J. J. Mol. Biol. 2008; 375: 1282-1292Crossref PubMed Scopus (12) Google Scholar).We observed that the presence of the negative charges in TM 2 and 3 determines the YidC-dependent insertion. NuoK contains single glutamates in TM2 and 3, which are required for high ubiquinone activity (35Kervinen M. Pätsi J. Finel M. Hassinen I.E. Biochemistry. 2004; 43: 773-781Crossref PubMed Scopus (47) Google Scholar, 36Kao M.C. Nakamaru-Ogiso E. Matsuno-Yagi A. Yagi T. Biochemistry. 2005; 44: 9545-9554Crossref PubMed Scopus (55) Google Scholar). Substitution of the glutamates at positions 36 and 72 for lysines produced a protein that, like most studied integral membrane proteins, required only SecYEG for integration into the membrane. This supports a model in which the TMSs of YidC have a role in forming a membrane chaperone, assisting the integration of less hydrophobic, negatively charged TMSs, similar to that proposed for Oxa1 (34Saint-Georges Y. Hamel P. Lemaire C. Dujardin G. Proc. Natl. Acad. Sci. U.S.A. 2001; 98: 13814-13819Crossref PubMed Scopus (20) Google Scholar, 34Saint-Georges Y. Hamel P. Lemaire C. Dujardin G. Proc. Natl. Acad. Sci. U.S.A. 2001; 98: 13814-13819Crossref PubMed Scopus (20) Google Scholar). The presence of just one glutamate-containing TMS renders the entire protein still YidC-dependent, and it is only when both glutamates have been substituted for lysines that the protein can be inserted by SecYEG, unassisted by YidC. NuoK is one of many integral membrane respiratory proteins that contain membrane-negative charges. NuoA has a similar structure to NuoK with glutamates at positions 81 and 102 (TM2 and 3) and an asparate at position 79 (TM2). It would be of interest if these similar structural features necessitate YidC in the insertion process.In the well studied substrate of YidC, Foc, mutation of an aspartate at position 61 (TM2) to a glycine produces an ATP synthase that contains an enzymatically active F1 part but no functional F0 (47Wachter E. Schmid R. Deckers G. Altendorf K. FEBS Lett. 1980; 113: 265-270Crossref PubMed Scopus (34) Google Scholar). There were, however, detectable levels of the mutant Foc present in the membrane. Attempts to elucidate the insertion requirements for this mutant in vitro were unsuccessful because of the proteinase K-resistant nature of the protein. 3S. Kol and J. de Keyzer, unpublished data. Substitution of a glycine for aspartate in TM1 of Foc results in a mutant form of the protein that is still dependent of YidC for insertion but that does not form an oligomeric ring structure as the wild type protein does (32Kol S. Turrell B.R. de Keyzer J. van der Laan M. Nouwen N. Driessen A.J. J. Biol. Chem. 2006; 281: 29762-29768Abstract Full Text Full Text PDF PubMed Scopus (29) Google Scholar, 48Jans D.A. Fimmel A.L. Langman L. James L.B. Downie J.A. Senior A.E. Ash G.R. Gibson F. Cox G.B. Biochem. J. 1983; 211: 717-726Crossref PubMed Scopus (34) Google Scholar). Thus the introduction of a negative charge into a TMS is tolerated by the YidC-only mode of insertion. Of the other proteins shown to insert with the assistance of YidC, the mechanosensitive channel of large conductance, MscL, and the phage coat proteins M13 and Pf3 have membrane-located negative charges. CyoA, however, does not contain any membrane-negative charges. YidC is not essential for the insertion of FtsQ (26van der Laan M. Nouwen N. Driessen A.J. J. Biol. Chem. 2004; 279: 1659-1664Abstract Full Text Full Text PDF PubMed Scopus (50) Google Scholar) and LepB (49de Gier J.W. Scotti P.A. Sääf A. Valent Q.A. Kuhn A. Luirink J. von Heijne G. Proc. Natl. Acad. Sci. U.S.A. 1998; 95: 14646-14651Crossref PubMed Scopus (112) Google Scholar), even though interaction between these proteins and YidC during membrane insertion has been observed (1Scotti P.A. Urbanus M.L. Brunner J. de Gier J.W. von Heijne G. van der Does C. Driessen A.J. Oudega B. Luirink J. EMBO J. 2000; 19: 542-549Crossref PubMed Scopus (299) Google Scholar, 24van der Laan M. Houben E.N. Nouwen N. Luirink J. Driessen A.J. EMBO Rep. 2001; 2: 519-523Crossref PubMed Scopus (95) Google Scholar, 42Yu Z. Koningstein G. Pop A. Luirink J. J. Biol. Chem. 2008; 283: 34635-34642Abstract Full Text Full Text PDF PubMed Scopus (35) Google Scholar, 43Beck K. Eisner G. Trescher D. Dalbey R.E. Brunner J. Müller M. EMBO Rep. 2001; 2: 709-714Crossref PubMed Scopus (136) Google Scholar, 50Houben E.N. Zarivach R. Oudega B. Luirink J. J. Cell Biol. 2005; 170: 27-35Crossref PubMed Scopus (47) Google Scholar). FtsQ does not contain any membrane-embedded charges, whereas LepB contains a glutamate in TM2. There must therefore be structural features other than membrane-located negative charges that confer YidC dependence to proteins.YidC is remarkably resilient to single amino acid substitutions, and even when TMSs 4 and 5 were swapped for unrelated TMSs, YidC activity was retained (33Jiang F. Chen M. Yi L. de Gier J.W. Kuhn A. Dalbey R.E. J. Biol. Chem. 2003; 278: 48965-48972Abstract Full Text Full Text PDF PubMed Scopus (81) Google Scholar). It has therefore been suggested that it is the presence of the C-terminal 5 TMSs and not the specific sequences of the hydrophobic stretches that is essential for YidC activity. Our data support the hypothesis that YidC serves as a platform from which TMSs are integrated into the membrane. Furthermore, YidC is essential for NuoK TMS integration when membrane-embedded negative charges are present. The involvement of YidC in the integration of such TMSs may provide an explanation as to its conserved function in the biogenesis of respiratory proteins that often contain essential-for-function negative charges providing a basis for future mutagenesis studies on other YidC substrates. IntroductionIn Escherichia coli the inner membrane contains essential energy transducing complexes such as components of the electron transport chain. The majority of inner membrane proteins are inserted cotranslationally via the general secretory pathway otherwise known as the Sec system. In this pathway, the bacterial signal recognition particle targets ribosome-bound nascent chains to the SecYEG translocase via the signal recognition particle receptor FtsY. Membrane insertion of these proteins proceeds by a cotranslational “threading mechanism” in which the accessory protein YidC is postulated to play an important role in the clearance of transmembrane segments (TMSs) 2The abbreviations used are: TMStransmembrane segmentIMVinner membrane vesiclePMFproton motive forceNTAnitrilotriacetic acid. from the SecYEG channel (1Scotti P.A. Urbanus M.L. Brunner J. de Gier J.W. von Heijne G. van der Does C. Driessen A.J. Oudega B. Luirink J. EMBO J. 2000; 19: 542-549Crossref PubMed Scopus (299) Google Scholar, 2de Gier J.W. Luirink J. Mol. Microbiol. 2001; 40: 314-322Crossref PubMed Scopus (82) Google Scholar). A small subset of integral membrane proteins are targeted directly to YidC where they are integrated into the membrane in a Sec-independent manner. YidC belongs to the evolutionarily conserved Oxa1/Alb3/YidC family. Oxa-related proteins have been identified in all genomes sequenced to date and are postulated to have evolved before the divergence of the three major domains of life (3Pohlschröder M. Hartmann E. Hand N.J. Dilks K. Haddad A. Annu. Rev. Microbiol. 2005; 59: 91-111Crossref PubMed Scopus (97) Google Scholar, 4Yen M.R. Harley K.T. Tseng Y.H. Saier Jr., M.H. FEMS Microbiol. Lett. 2001; 204: 223-231Crossref PubMed Google Scholar, 5Luirink J. Samuelsson T. de Gier J.W. FEBS Lett. 2001; 501: 1-5Crossref PubMed Scopus (121) Google Scholar). Oxa1 (oxidase assembly) from yeast was the first member of this family to be described (6Bauer M. Behrens M. Esser K. Michaelis G. Pratje E. Mol. Gen. Genet. 1994; 245: 272-278Crossref PubMed Scopus (106) Google Scholar, 7Bonnefoy N. Chalvet F. Hamel P. Slonimski P.P. Dujardin G. J. Mol. Biol. 1994; 239: 201-212Crossref PubMed Scopus (179) Google Scholar). It was originally identified as an essential factor for the biogenesis of respiratory complexes in the mitochondrion, more specifically for the insertion of subunits of the cytochrome bc1 oxidase and ATP synthase (8Altamura N. Capitanio N. Bonnefoy N. Papa S. Dujardin G. FEBS Lett. 1996; 382: 111-115Crossref PubMed Scopus (124) Google Scholar). Alb3 is located in the thylakoid membranes of plant chloroplasts and involved in the biogenesis of light harvesting complexes (9Moore M. Harrison M.S. Peterson E.C. Henry R. J. Biol. Chem. 2000; 275: 1529-1532Abstract Full Text Full Text PDF PubMed Scopus (184) Google Scholar). In E. coli it has been shown that YidC is essential for the insertion of subunit c and a of the F1F0 ATP synthase (Foc and Foa) (10van der Laan M. Bechtluft P. Kol S. Nouwen N. Driessen A.J. J. Cell Biol. 2004; 165: 213-222Crossref PubMed Scopus (174) Google Scholar, 11Yi L. Jiang F. Chen M. Cain B. Bolhuis A. Dalbey R.E. Biochemistry. 2003; 42: 10537-10544Crossref PubMed Scopus (100) Google Scholar), subunit a of cytochrome o oxidase (CyoA) (12du Plessis D.J. Nouwen N. Driessen A.J. J. Biol. Chem. 2006; 281: 12248-12252Abstract Full Text Full Text PDF PubMed Scopus (71) Google Scholar, 13van Bloois E. Haan G.J. de Gier J.W. Oudega B. Luirink J. J. Biol. Chem. 2006; 281: 10002-10009Abstract Full Text Full Text PDF PubMed Scopus (64) Google Scholar), and MscL, the mechanosensitive channel of large conductance (14Facey S.J. Neugebauer S.A. Krauss S. Kuhn A. J. Mol. Biol. 2007; 365: 995-1004Crossref PubMed Scopus (90) Google Scholar).Although members of the family have all been implicated in membrane protein biogenesis of respiratory and energy transducing proteins, there is a great variance in substrate specificity within the family. For example Oxa1 proteins appear to have a varying role in the biogenesis of respiratory complexes I, III, IV, and V as illustrated by studies in Neurospora crassa, (15Nargang F.E. Preuss M. Neupert W. Herrmann J.M. J. Biol. Chem. 2002; 277: 12846-12853Abstract Full Text Full Text PDF PubMed Scopus (74) Google Scholar), Podospora anseria (16Sellem C.H. Lemaire C. Lorin S. Dujardin G. Sainsard-Chanet A. Genetics. 2005; 169: 1379-1389Crossref PubMed Scopus (26) Google Scholar), HEK293 cells (17Stiburek L. Fornuskova D. Wenchich L. Pejznochova M. Hansikova H. Zeman J. J. Mol. Biol. 2007; 374: 506-516Crossref PubMed Scopus (67) Google Scholar), and Saccharomyces cerevisiae (6Bauer M. Behrens M. Esser K. Michaelis G. Pratje E. Mol. Gen. Genet. 1994; 245: 272-278Crossref PubMed Scopus (106) Google Scholar, 7Bonnefoy N. Chalvet F. Hamel P. Slonimski P.P. Dujardin G. J. Mol. Biol. 1994; 239: 201-212Crossref PubMed Scopus (179) Google Scholar, 18Meyer W. Bauer M. Pratje E. Curr. Genet. 1997; 31: 401-407Crossref PubMed Scopus (22) Google Scholar, 19Lemaire C. Hamel P. Velours J. Dujardin G. J. Biol. Chem. 2000; 275: 23471-23475Abstract Full Text Full Text PDF PubMed Scopus (59) Google Scholar, 20Jia L. Dienhart M.K. Stuart R.A. Mol. Biol. Cell. 2007; 18: 1897-1908Crossref PubMed Scopus (79) Google Scholar). This highlights that although the general function of Oxa1/Alb3/YidC family proteins is known, each member plays a specific and in some cases yet to be identified role in the biogenesis of respiratory proteins.In a recent study, we showed that YidC depletion in E. coli resulted in a cessation of growth under anaerobic conditions and that this growth defect may be in part due to reduced levels of the complex I homolog in bacteria, the NADH:ubiquinone reductase, or NADH dehydrogenase I, in the membrane (21Price C.E. Driessen A.J. J. Biol. Chem. 2008; 283: 26921-26927Abstract Full Text Full Text PDF PubMed Scopus (27) Google Scholar). In particular, levels of the smallest membrane subunit K (NuoK) decreased. The aim of this study was to elucidate the role of YidC in NuoK membrane biogenesis and to determine the structural features of NuoK underlying this role. We found that in vitro synthesized NuoK requires both SecYEG and YidC for insertion and that two conserved negative charges in TMSs 2 and 3 determine the dependence of NuoK on YidC for insertion. In Escherichia coli the inner membrane contains essential energy transducing complexes such as components of the electron transport chain. The majority of inner membrane proteins are inserted cotranslationally via the general secretory pathway otherwise known as the Sec system. In this pathway, the bacterial signal recognition particle targets ribosome-bound nascent chains to the SecYEG translocase via the signal recognition particle receptor FtsY. Membrane insertion of these proteins proceeds by a cotranslational “threading mechanism” in which the accessory protein YidC is postulated to play an important role in the clearance of transmembrane segments (TMSs) 2The abbreviations used are: TMStransmembrane segmentIMVinner membrane vesiclePMFproton motive forceNTAnitrilotriacetic acid. from the SecYEG channel (1Scotti P.A. Urbanus M.L. Brunner J. de Gier J.W. von Heijne G. van der Does C. Driessen A.J. Oudega B. Luirink J. EMBO J. 2000; 19: 542-549Crossref PubMed Scopus (299) Google Scholar, 2de Gier J.W. Luirink J. Mol. Microbiol. 2001; 40: 314-322Crossref PubMed Scopus (82) Google Scholar). A small subset of integral membrane proteins are targeted directly to YidC where they are integrated into the membrane in a Sec-independent manner. YidC belongs to the evolutionarily conserved Oxa1/Alb3/YidC family. Oxa-related proteins have been identified in all genomes sequenced to date and are postulated to have evolved before the divergence of the three major domains of life (3Pohlschröder M. Hartmann E. Hand N.J. Dilks K. Haddad A. Annu. Rev. Microbiol. 2005; 59: 91-111Crossref PubMed Scopus (97) Google Scholar, 4Yen M.R. Harley K.T. Tseng Y.H. Saier Jr., M.H. FEMS Microbiol. Lett. 2001; 204: 223-231Crossref PubMed Google Scholar, 5Luirink J. Samuelsson T. de Gier J.W. FEBS Lett. 2001; 501: 1-5Crossref PubMed Scopus (121) Google Scholar). Oxa1 (oxidase assembly) from yeast was the first member of this family to be described (6Bauer M. Behrens M. Esser K. Michaelis G. Pratje E. Mol. Gen. Genet. 1994; 245: 272-278Crossref PubMed Scopus (106) Google Scholar, 7Bonnefoy N. Chalvet F. Hamel P. Slonimski P.P. Dujardin G. J. Mol. Biol. 1994; 239: 201-212Crossref PubMed Scopus (179) Google Scholar). It was originally identified as an essential factor for the biogenesis of respiratory complexes in the mitochondrion, more specifically for the insertion of subunits of the cytochrome bc1 oxidase and ATP synthase (8Altamura N. Capitanio N. Bonnefoy N. Papa S. Dujardin G. FEBS Lett. 1996; 382: 111-115Crossref PubMed Scopus (124) Google Scholar). Alb3 is located in the thylakoid membranes of plant chloroplasts and involved in the biogenesis of light harvesting complexes (9Moore M. Harrison M.S. Peterson E.C. Henry R. J. Biol. Chem. 2000; 275: 1529-1532Abstract Full Text Full Text PDF PubMed Scopus (184) Google Scholar). In E. coli it has been shown that YidC is essential for the insertion of subunit c and a of the F1F0 ATP synthase (Foc and Foa) (10van der Laan M. Bechtluft P. Kol S. Nouwen N. Driessen A.J. J. Cell Biol. 2004; 165: 213-222Crossref PubMed Scopus (174) Google Scholar, 11Yi L. Jiang F. Chen M. Cain B. Bolhuis A. Dalbey R.E. Biochemistry. 2003; 42: 10537-10544Crossref PubMed Scopus (100) Google Scholar), subunit a of cytochrome o oxidase (CyoA) (12du Plessis D.J. Nouwen N. Driessen A.J. J. Biol. Chem. 2006; 281: 12248-12252Abstract Full Text Full Text PDF PubMed Scopus (71) Google Scholar, 13van Bloois E. Haan G.J. de Gier J.W. Oudega B. Luirink J. J. Biol. Chem. 2006; 281: 10002-10009Abstract Full Text Full Text PDF PubMed Scopus (64) Google Scholar), and MscL, the mechanosensitive channel of large conductance (14Facey S.J. Neugebauer S.A. Krauss S. Kuhn A. J. Mol. Biol. 2007; 365: 995-1004Crossref PubMed Scopus (90) Google Scholar). transmembrane segment inner membrane vesicle proton motive force nitrilotriacetic acid. Although members of the family have all been implicated in membrane protein biogenesis of respiratory and energy transducing proteins, there is a great variance in substrate specificity within the family. For example Oxa1 proteins appear to have a varying role in the biogenesis of respiratory complexes I, III, IV, and V as illustrated by studies in Neurospora crassa, (15Nargang F.E. Preuss M. Neupert W. Herrmann J.M. J. Biol. Chem. 2002; 277: 12846-12853Abs" @default.
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• W2015761041 title "Conserved Negative Charges in the Transmembrane Segments of Subunit K of the NADH:Ubiquinone Oxidoreductase Determine Its Dependence on YidC for Membrane Insertion" @default.
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