Multiple variants of the human presequence translocase motor subunit Magmas govern the mitochondrial import

Abstract

Mitochondrial protein translocation is an intricately regulated process that requires dedicated translocases at the outer and inner membranes. The presequence translocase complex, translocase of the inner membrane 23, facilitates most of the import of preproteins containing presequences into the mitochondria, and its primary structural organization is highly conserved. As part of the translocase motor, two J-proteins, DnaJC15 and DnaJC19, are recruited to form two independent translocation machineries (translocase A and translocase B, respectively). On the other hand, the J-like protein subunit of translocase of the inner membrane 23, Mitochondria-associated granulocyte-macrophage colony-stimulating factor signaling molecule (Magmas) (orthologous to the yeast subunit Pam16), can regulate human import-motor activity by forming a heterodimer with DnaJC19 and DnaJC15. However, the precise coordinated regulation of two human import motors by a single Magmas protein is poorly understood. Here, we report two additional Magmas variants (Magmas-1 and Magmas-2) constitutively expressed in the mammalian system. Both the Magmas variants are functional orthologs of Pam16 with an evolutionarily conserved J-like domain critical for cell survival. Moreover, the Magmas variants are peripherally associated with the inner membrane as part of the human import motor for translocation. Our results demonstrate that Magmas-1 is predominantly recruited to translocase B, whereas Magmas-2 is majorly associated with translocase A. Strikingly, both the variants exhibit differential J-protein inhibitory activity in modulating import motor, thereby regulating overall translocase function. Based on our findings, we hypothesize that additional Magmas variants are of evolutionary significance in humans to maximize protein import in familial-linked pathological conditions. Mitochondrial protein translocation is an intricately regulated process that requires dedicated translocases at the outer and inner membranes. The presequence translocase complex, translocase of the inner membrane 23, facilitates most of the import of preproteins containing presequences into the mitochondria, and its primary structural organization is highly conserved. As part of the translocase motor, two J-proteins, DnaJC15 and DnaJC19, are recruited to form two independent translocation machineries (translocase A and translocase B, respectively). On the other hand, the J-like protein subunit of translocase of the inner membrane 23, Mitochondria-associated granulocyte-macrophage colony-stimulating factor signaling molecule (Magmas) (orthologous to the yeast subunit Pam16), can regulate human import-motor activity by forming a heterodimer with DnaJC19 and DnaJC15. However, the precise coordinated regulation of two human import motors by a single Magmas protein is poorly understood. Here, we report two additional Magmas variants (Magmas-1 and Magmas-2) constitutively expressed in the mammalian system. Both the Magmas variants are functional orthologs of Pam16 with an evolutionarily conserved J-like domain critical for cell survival. Moreover, the Magmas variants are peripherally associated with the inner membrane as part of the human import motor for translocation. Our results demonstrate that Magmas-1 is predominantly recruited to translocase B, whereas Magmas-2 is majorly associated with translocase A. Strikingly, both the variants exhibit differential J-protein inhibitory activity in modulating import motor, thereby regulating overall translocase function. Based on our findings, we hypothesize that additional Magmas variants are of evolutionary significance in humans to maximize protein import in familial-linked pathological conditions. In eukaryotic organisms, the organellar compartmentalization of cellular processes ensures metabolic homeostasis. Mitochondria are indispensable organelles vital for several cellular functions, including oxidative phosphorylation, β oxidation, iron-sulfur cluster biogenesis, and cell death (1Hatefi Y. The mitochondrial electron transport and oxidative phosphorylation system.Annu. Rev. Biochem. 1985; 54: 1015-1069Crossref PubMed Google Scholar, 2Schulz H. Beta oxidation of fatty acids.Biochim. Biophys. Acta. 1991; 1081: 109-120Crossref PubMed Scopus (286) Google Scholar, 3Lill R. Muhlenhoff U. Iron-sulfur-protein biogenesis in eukaryotes.Trends Biochem. Sci. 2005; 30: 133-141Abstract Full Text Full Text PDF PubMed Scopus (294) Google Scholar, 4Petit P.X. Susin S.A. Zamzami N. Mignotte B. Kroemer G. Mitochondria and programmed cell death: Back to the future.FEBS Lett. 1996; 396: 7-13Crossref PubMed Scopus (450) Google Scholar). The mitochondrial genome encodes only 8 and 13 proteins in yeast and humans, respectively. Hence, most mitochondrial protein repertoire is synthesized on the cytoplasmic ribosomes and subsequently imported into the organelle by organized protein-import machinery (5Hoogenraad N.J. Ryan M.T. Translocation of proteins into mitochondria.IUBMB Life. 2001; 51: 345-350Crossref PubMed Scopus (16) Google Scholar). The mitochondrial precursor proteins with targeting sequence (MTS) are recognized by the translocase of the outer membrane (TOM) and inner membrane (TIM). TIM23 (also known as presequence translocase) is a dynamic complex owing to the import of precursor proteins into the matrix, inner membrane (IM), and intermembrane space (IMS) (6Mokranjac D. Neupert W. The many faces of the mitochondrial TIM23 complex.Biochim. Biophys. Acta. 2010; 1797: 1045-1054Crossref PubMed Scopus (78) Google Scholar, 7Bolender N. Sickmann A. Wagner R. Meisinger C. Pfanner N. Multiple pathways for sorting mitochondrial precursor proteins.EMBO Rep. 2008; 9: 42-49Crossref PubMed Scopus (233) Google Scholar, 8Pfanner N. Geissler A. Versatility of the mitochondrial protein import machinery.Nat. Rev. Mol. Cell Biol. 2001; 2: 339-349Crossref PubMed Scopus (415) Google Scholar). The basic architecture of the TIM23 complex has remained conserved from yeast to humans. In Saccharomyces cerevisiae, there are two separate complex assemblies required for the matrix and IM sorting. The lateral IM sorting is performed by the core components of the TIM23 complex together with Tim21 and Mgr2 subunits (9Mokranjac D. Popov-Celeketic D. Hell K. Neupert W. Role of Tim21 in mitochondrial translocation contact sites.J. Biol. Chem. 2005; 280: 23437-23440Abstract Full Text Full Text PDF PubMed Scopus (90) Google Scholar, 10Gebert R. K. C. B. B. of the mitochondrial presequence translocase to Cell Biol. PubMed Scopus Google Scholar). The matrix import is by the of the core and import-motor subunit W. Translocation of proteins into Rev. Biochem. PubMed Scopus Google Scholar). The core of the membrane and The membrane protein is required for the of from the The a that the to the whereas the structural and of the Y. Y. K. K. H. H. of and motor proteins in mitochondrial protein Cell Biol. PubMed Scopus Google Scholar, D. S.A. C. H. Neupert W. Hell K. a of the TIM23 translocase of PubMed Scopus Google Scholar, the and of the mitochondrial protein import complex Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar, G. of and subunits of presequence Cell Biol. PubMed Scopus Google Scholar). The of the precursor proteins into the matrix is by the membrane IM by the of the import motor for translocation. The import is performed by the import-motor complex, subunits are highly conserved N. Pfanner N. The mitochondrial import machinery for Rev. Biochem. Mol. Biol. 2001; PubMed Scopus Google Scholar). Mitochondrial protein in the core of the import motor to the TIM23 peripherally associated W. of with at the in the mitochondrial inner Mol. Biol. PubMed Scopus Google Scholar). The with the of the in an activity is by a thereby the of the to the matrix W. The protein import motor of Rev. Mol. Cell Biol. PubMed Scopus Google Scholar, W. of mitochondrial at the protein import PubMed Scopus Google Scholar, B. W. A. protein of the mitochondrial inner membrane required for protein import into the mitochondrial Sci. U. A. PubMed Scopus Google Scholar). The of with the J-like domain the import-motor thereby the of the import B. W. Y. Meisinger C. Geissler A. Sickmann A. Pfanner N. Pam16 has an in the mitochondrial protein import Mol. Biol. PubMed Scopus Google Scholar, C. D. Neupert W. Hell K. The is a of the mitochondrial TIM23 Mol. Biol. PubMed Scopus Google Scholar, B. of the J-protein heterodimer of the mitochondrial import motor with the of the inner Biol. 2008; PubMed Scopus Google Scholar). The the form of to the of the import-motor activity B. Neupert W. The factor a in the of mitochondrial protein 1996; PubMed Scopus Google Scholar). the primary organization of the TIM23 complex to conserved there are to and of the human mitochondrial import system. The structural of the TIM23 subunits are in yeast with the of a single presequence translocase However, humans to TIM23 is of the of additional variants of components of the TIM23 in and as subunits of separate TIM23 K. Neupert W. and structural of the human mitochondrial inner membrane Mol. Biol. PubMed Scopus Google Scholar, D. the organization of mammalian mitochondrial presequence of translocases for of mitochondrial Cell Biol. PubMed Scopus Google Scholar). the as of yeast in two in humans with functions, and N.J. for the of mammalian and two mitochondrial the of Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar, D. A. of mitochondrial protein import by the and in human Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar). On the other hand, humans to two J-proteins, DnaJC19 and of single in yeast A. R. of a human of yeast inner mitochondrial membrane a PubMed Scopus Google Scholar, C. A. Hell K. J-protein in the import of proteins into human Mol. PubMed Scopus Google Scholar). and J-like proteins as a the of two in humans the regulation by a single form of the human of J-like Magmas of Mitochondria-associated granulocyte-macrophage colony-stimulating factor signaling molecule (Magmas) as a protein The of Magmas the cell in the of A. and of a protein in granulocyte-macrophage colony-stimulating factor 2001; Full Text Full Text PDF PubMed Scopus Google Scholar). The protein of Magmas the in the and G. of Magmas in and its with the 51: PubMed Scopus Google Scholar). a critical the Magmas as a functional of yeast a subunit of human import motor D. N. B. Role of Magmas in protein transport and human Mol. 2010; PubMed Scopus Google Scholar, D. A. The mitochondrial protein translocation the human and yeast Mol. Sci. PubMed Scopus Google Scholar). the of Magmas whereas the J-like domain the Magmas to the of the conserved at the is by D. D. The J-protein protein and Rep. PubMed Scopus Google Scholar). Magmas the activity of in and as a with J-proteins, DnaJC19 and by regulating the import-motor activity at the presequence translocase machinery B. W. Role of domain in protein import the mitochondrial inner Sci. U. A. 2005; PubMed Scopus Google Scholar, D. of human mitochondrial is independent of with the inner membrane presequence Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar). The Magmas is for the of C. and its in A. The of a conserved protein and is required for and 2001; PubMed Scopus Google Scholar, C. K. A. K. A. of cell in C. of on PubMed Scopus Google Scholar). from the primary protein import Magmas to additional in as a signaling The of Magmas is in including and N. A. G. and A of in the Scopus Google Scholar, K. N. Magmas as a in PubMed Scopus Google Scholar, G. Magmas in human Mol. 2005; PubMed Scopus Google Scholar). Moreover, Magmas in the in and the from D. a as in human and from 2010; PubMed Scopus Google Scholar, D. Magmas in cell Google Scholar). In human the Magmas oxidative by regulating the D. H. Magmas as a and oxidative PubMed Scopus Google Scholar). In a Magmas in in and cell of is by its on mitochondrial PubMed Scopus Google Scholar). in two of Pam16 and that are required for the mitochondrial import and Y. Y. C. C. Mitochondrial is required for and the regulation of PubMed Scopus Google Scholar, C. C. of the evolutionarily conserved of proteins in the mitochondrial import Mol. Biol. PubMed Scopus Google Scholar). Hence, the additional with an regulating Magmas in the mammalian and its in with in pathological conditions. In the we the of two additional Magmas variants in humans. Both the variants of Magmas are recruited to the separate TIM23 machinery regulating import-motor functions, the of translocation machinery at the mitochondrial Our to that Magmas variants regulate the import-motor the significance of the of the in and pathological conditions. The TIM23 complex is an IM translocase for the and sorting of a for the biogenesis of matrix proteins by the membrane and import the basic architecture of the TIM23 complex has remained conserved the the organization of the mammalian is The human TIM23 complex is by the of subunits of protein in humans is the DnaJC19 and DnaJC15. Both the form a with the Magmas and are organized into separate translocation two J-protein a single Magmas protein is an the of additional Magmas variants in regulating the protein import process in humans, we performed sequence with the Magmas the two with the of the as a at whereas the other with a sequence as Magmas-2) the of variants at the cellular we at both and protein from human cell by with the the at an the of Magmas variants the several Magmas and and for and as Magmas-1 and respectively. the of we performed sequence of the other variants with in sequence In we the the in of from human cell The protein the the Magmas the the J-like domain the of two Magmas variants However, of the in the and we only two of the variants in the The for the of Magmas only two we the other variants of Magmas on the from the we an the and of Magmas-1 and the of variants in cell and In our results the of two Magmas Magmas-1 and in human cell that are as a of The J-like Pam16 of cerevisiae, has as an of Magmas D. N. B. Role of Magmas in protein transport and human Mol. 2010; PubMed Scopus Google Scholar). to the Magmas-1 and Magmas-2 in we the The of Magmas variants performed by the The Magmas variants expressed in yeast and into with Pam16 in a The on the the of of The on and to on and As Magmas the of the Magmas-1 and Magmas-2 yeast cell Pam16 at the on and The as a that Magmas variants are The of variants is by The Magmas-1 and Magmas-2 in the The of variants in the yeast with that and with the variants in yeast that the of Pam16 a functional heterodimer with B. W. Role of domain in protein import the mitochondrial inner Sci. U. A. 2005; PubMed Scopus Google Scholar, D. G. Hell K. Neupert W. and of and the and J-like components of the mitochondrial protein import PubMed Scopus Google Scholar). In of Pam16 has remained conserved the in its in mitochondrial D. N. B. Role of Magmas in protein transport and human Mol. 2010; PubMed Scopus Google Scholar). to the significance in the we a and performed on and and a to and functional of in the variants The of proteins by to the of the conserved J-like domain of we a the of the J-like at of Magmas to in Magmas-1 and Magmas-2 to the and a in and with as D. N. B. Role of Magmas in protein transport and human Mol. 2010; PubMed Scopus Google Scholar, K. R. The yeast has an in that PubMed Scopus Google Scholar). In and at the in with and a at the on and The of by results the functional of the J-like domain in Magmas and in are critical for cellular Magmas and Pam16 to at the IM of B. W. Y. Meisinger C. Geissler A. Sickmann A. Pfanner N. Pam16 has an in the mitochondrial protein import Mol. Biol. PubMed Scopus Google Scholar, C. D. Neupert W. Hell K. The is a of the mitochondrial TIM23 Mol. Biol. PubMed Scopus Google Scholar). we for the and of Magmas-1 and Magmas-2 by and we Magmas variants at the of in the and expressed in and cell A and B, Mitochondria with constitutively to of A and B, and Magmas-2 to with the with a in the mitochondrial targeting of the variants in the mammalian A and B, in the mitochondrial of precise mitochondrial we performed of from yeast and to the IM we in and by and membrane by and on The of Pam16 and Magmas with the and The Magmas-1 and with the membrane to peripherally associated IM and As a an IM in the On the other hand, matrix proteins and from human and yeast mitochondria, as for the and the variants are associated peripherally into the the from yeast and to at Both Pam16 and Magmas to the with the and On the other hand, of Magmas-1 and together with in the by and The protein as an membrane that remained in the that Magmas variants are peripherally associated with the IM of the The presequence translocase at the IM of is for matrix proteins and IM sorting. of TIM23 core complex and peripherally associated import-motor Pam16 is to to the TIM23 complex its J-like domain by forming a heterodimer with whereas the with B. of the J-protein heterodimer of the mitochondrial import motor with the of the inner Biol. 2008; PubMed Scopus Google Scholar, of complex components of the mitochondrial import motor and in Saccharomyces PubMed Scopus Google Scholar). the Magmas with two J-protein and to form separate at the human import motor, thereby into of the presequence translocase machinery D. the organization of mammalian mitochondrial presequence of translocases for of mitochondrial Cell Biol. PubMed Scopus Google Scholar, D. of human mitochondrial is independent of with the inner membrane presequence Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar). the of Magmas variants with translocation machinery in both yeast and humans, we performed a and Mitochondria from yeast Magmas-2 for The mitochondrial by by the of with protein The Pam16 and Magmas with TIM23 complex components as and with On the other hand, Magmas-1 and Magmas-2 variants with the TIM23 complex the functional at the import motor the of as a of TIM23 subunits the of Magmas variants with human J-proteins, DnaJC19 and we performed The in by the of variants with the of The Magmas with both and B, and On the other hand, both the variants with However, Magmas-2 with to a B, and The as a of with J-proteins, the in of Magmas variants in the of other TIM23 complex components to the with the human TIM23 complex, we performed a with Magmas Magmas to with TIM23 complex including and and the DnaJC19 and DnaJC15 on the other hand, Magmas-1 predominantly associated with the TIM23 complex containing and DnaJC19, that majorly a part of presequence translocase machinery the Magmas-2 majorly associated with the TIM23 complex containing the and its in presequence translocase A machinery components of the TIM23 complex, and in in the of Magmas variants to the presequence translocase The and a of outer membrane complex, as a a of components of the TIM23 complex In our results that the Magmas variants with the yeast presequence translocase and are recruited to human TIM23 of Pam16 and Magmas as a part of the import motor of the TIM23 The are import motor, J-like proteins regulate J-protein thereby the precursor in the import motor the mitochondrial matrix import to the of precursor proteins in the The Magmas mitochondrial matrix protein import in with its to the the we performed a precursor with Magmas-1 and Magmas-2 two yeast mitochondrial matrix and to in precursor G. K. A. Role of in regulating the architecture of presequence translocase and mitochondrial Cell Biol. PubMed Scopus Google Scholar). with Pam16 Magmas variants the and to The cell on by with and The Magmas variants a of and A and On the other hand, the Magmas as an to demonstrate the precursor an import A and B, two The results that the Magmas variants can import as a part of the subunit of the TIM23 complex by the of protein translocation into the mitochondrial matrix, we performed in import with protein as B. Pfanner N. W. The mitochondrial import preproteins and the of 2001; PubMed Scopus Google Scholar). The from and its variants yeast with the of protein for the import Both Magmas-1 and Magmas-2 exhibit in the import to and Pam16 that Magmas variants at the yeast import motor and The is a and requires the J-protein to the activity and the import DnaJC19 and DnaJC15 to the of at the human presequence translocase and D. of human mitochondrial is independent of with the inner membrane presequence Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar). Magmas thereby regulating the import-motor function. Magmas variants with the human TIM23 complex, we inhibitory on the import we performed the single a by the of A and On the other hand, Magmas to to of activity with A and However, at Magmas variants differential inhibitory The Magmas-1 inhibitory activity with Magmas A and on the other hand, Magmas-2 with Magmas and Magmas-1 A and The differential inhibitory that Magmas variants a in regulating the import motor of the TIM23 results in the of the of the J-protein to a in the activity of and to to by the of whereas Magmas-1 to inhibitory on the activity and the of Magmas-2 the thereby the inhibitory of and In Magmas variants the activity of in the of a in regulating the import In eukaryotic is a highly regulated process import of outer membrane and complex machinery is the TIM23 complex, required for the of and Our of the presequence import process is the of the is from as a system. On the other hand, in the mammalian several of the TIM23 complex at the IM of the of subunit and for the of pathological conditions. The the of two additional variants of Magmas that regulate the human presequence translocase Our of the functional of Magmas variants with cerevisiae, Pam16 single Pam16 from the to variants in humans, the overall J-like domain remained by our in the yeast system. The Magmas variants are to mitochondrial IM by peripherally with the yeast TIM23 structural of Magmas variants with yeast TIM23 complex in the of import-motor as by in precursor and in import the of TIM23 on Magmas variants is predominantly associated with of presequence translocase machinery the of Magmas variants in regulating the import-motor activity the significance of Magmas to in several the of Magmas variants with of significance in mitochondrial on the presequence translocase machinery an of the of a single complex from yeast to separate translocases in humans translocase and translocase Our in Magmas can with both translocase A and the Magmas-1 is predominantly associated with the components of translocase machinery On the other hand, Magmas-2 is majorly associated with translocase A However, our a of translocase A in Magmas-1 and translocase in we hypothesize that the Magmas as a constitutively primary the on additional in Magmas-1 and Magmas-2 can the import-motor The Magmas variants an in humans, the presequence translocase machinery is indispensable for cellular whereas translocase A has a D. the organization of mammalian mitochondrial presequence of translocases for of mitochondrial Cell Biol. PubMed Scopus Google Scholar). Based on our findings, we that Magmas-1 predominantly in a in functions, whereas Magmas-2 is majorly in pathological as the TIM23 complex, the conserved J-like domain at the of Magmas variants a with the of the the activity of regulating the import-motor function. In the of a J-like domain to of activity with both the is to that a of and the J-like domain the overall activity of the Magmas-2 the of the of the at the on the J-like many of the Magmas variants remained evolutionarily we that at the and the overall of the TIM23 complex in humans. the of Magmas and variants in overall cell and mitochondrial biogenesis is critical to its differential in metabolic G. of Magmas in and its with the 51: PubMed Scopus Google Scholar). The Magmas is in including and N. A. G. and A of in the Scopus Google Scholar, G. Magmas in human Mol. 2005; PubMed Scopus Google Scholar, D. a as in human and from 2010; PubMed Scopus Google Scholar). independent mitochondrial of from the protein its as a signaling molecule K. N. Magmas as a in PubMed Scopus Google Scholar). Magmas to a as a by oxidative and its is required for D. H. Magmas as a and oxidative PubMed Scopus Google Scholar, Y. Y. C. C. Mitochondrial is required for and the regulation of PubMed Scopus Google Scholar). that the in a Magmas J-like domain with mitochondrial import in humans C. A. N. A. A. The of in human is for a PubMed Scopus Google Scholar, H. G. B. A in a with a and A. PubMed Scopus Google Scholar). are in the of the in humans Pam16 and its orthologs as Magmas are for cell in humans, is that the Magmas-1 can the Magmas as a part of the import motor at the presequence is for the mammalian system. a single in DnaJC19 of in the of with A. R. of a human of yeast inner mitochondrial membrane a PubMed Scopus Google Scholar). the at the import motor, thereby the import and mitochondrial variants of Magmas as a part of translocase machinery highly to maximize the import the of evolutionary the DnaJC15 J-protein of in to in R. K. H. of of a of the protein to in the of 2001; Google Scholar, G. N. R. of the in and to 2005; Full Text Full Text PDF PubMed Scopus Google Scholar). A to the Magmas in as a K. N. Magmas as a in PubMed Scopus Google Scholar). Magmas variants several in mitochondrial as an additional the there are other functional of variants to in the are in the mitochondrial in pathological as In the TIM23 in human mitochondria, its structural organization Our of Magmas variants the of presequence translocase machinery regulating the protein import the human mitochondrial Moreover, our vital into the human import motor at the presequence the variants to in pathological conditions. and in with and in with the components of and performed as the in in of The Magmas variants in Pam16 in and subsequently on The on to the of The the Magmas variants for on and and other The with by the The to the The for the of Magmas variants from and The Magmas variants and Pam16 in the the to the yeast and Magmas-2 as protein by respectively. performed of the Magmas variants at the of in the The Magmas-1 and Magmas-2 the and and primary in are D. the organization of mammalian mitochondrial presequence of translocases for of mitochondrial Cell Biol. PubMed Scopus Google Scholar). and the J-like and whereas the In for yeast and by A. and the and respectively. and with Magmas variants protein and of the and human as C. from and 2: PubMed Scopus Google Scholar, A. Mgr2 mitochondrial import by with Biol. PubMed Google Scholar). of yeast and of human to in and for to the whereas for protein by the to at for at The and on and the proteins of by of and as D. N. B. Role of Magmas in protein transport and human Mol. 2010; PubMed Scopus Google Scholar, D. of human mitochondrial is independent of with the inner membrane presequence Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar). The Magmas variants by with the Magmas variants to the The by the of for at Cell in of A and containing and for at The with for at by at The and by at for and the with for at The proteins by with A containing by a with and by the with and proteins in the and the of The proteins and to the with a proteins expressed in and of proteins with Biochem. 1991; PubMed Scopus Google Scholar). of in the the of the yeast TIM23 complex, of to in and containing The at for at to the The for with primary protein at the in a containing by on and by with the of Magmas variants with A and for at by with for at variants with of for at The with A and to by mitochondria, from with and containing for conditions. for the with for at The proteins by with The on and by the of precursor protein in the yeast proteins to the The to at for The cell and by and In import as B. Pfanner N. W. The mitochondrial import preproteins and the of 2001; PubMed Scopus Google Scholar). The in a matrix targeting by the with the of of with the The by the of by The J-proteins, DnaJC19 and with the and and A complex of with with and the Magmas variants in the of at The by and in the at on the and by by in is in the The that of with the of A. for yeast and are to for critical into the and W. and D. W. and D. W. and D. W. and D. W. W. W. W. D. D. D. D. and by and D. the of and

Topics & Concepts