Membrane protein insertion: mixing eukaryotic and prokaryotic concepts

Proteins are translocated across or inserted into membranes by machines that are composed of soluble and membrane‐anchored subunits. The molecular action of these machines and their evolutionary origin are at present the focus of intense research. For instance, our understanding of the mode of insertion of β‐barrel membrane proteins into the outer membrane of endosymbiotically derived organelles has increased rapidly during the past few years. In particular, the identification of the Omp85/YaeT‐involving pathways in Neisseria meningitidis, Escherichia coli and cyanobacteria, and homologues of Omp85/YaeT in chloroplasts and mitochondria, has provided new clues about the ancestral β‐barrel protein insertion pathway. This review focuses on recent advances in the elucidation of the evolutionarily conserved concepts that underlie the translocation and insertion of β‐barrel membrane proteins.

[1]  V. Braun,et al.  Activation of Serratia marcescens Hemolysin through a Conformational Change , 2004, Infection and Immunity.

[2]  V. Braun,et al.  Subcellular location and unique secretion of the hemolysin of Serratia marcescens. , 1989, The Journal of biological chemistry.

[3]  P. Tranel,et al.  A novel, bipartite transit peptide targets OEP75 to the outer membrane of the chloroplastic envelope. , 1996, The Plant cell.

[4]  E. Schleiff,et al.  Without a little help from 'my' friends: direct insertion of proteins into chloroplast membranes? , 2001, Biochimica et biophysica acta.

[5]  Walter Neupert,et al.  Evolutionary conservation of biogenesis of β-barrel membrane proteins , 2003, Nature.

[6]  A. Schulz,et al.  Origin of a chloroplast protein importer. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[7]  T. Lithgow,et al.  The alpha and the beta: protein translocation across mitochondrial and plastid outer membranes. , 2001, Trends in biochemical sciences.

[8]  A. von Haeseler,et al.  Conserved pore‐forming regions in polypeptide‐ transporting proteins , 2005, The FEBS journal.

[9]  N. Walter,et al.  Mim1, a protein required for the assembly of the TOM complex of mitochondria , 2005 .

[10]  C. Gross,et al.  Characterization of Six Lipoproteins in the σE Regulon , 2005 .

[11]  B. Schönfisch,et al.  Machinery for protein sorting and assembly in the mitochondrial outer membrane , 2003, Nature.

[12]  Enrico Schleiff,et al.  Protein import into chloroplasts , 2004, Nature Reviews Molecular Cell Biology.

[13]  P. Tranel,et al.  A component of the chloroplastic protein import apparatus is targeted to the outer envelope membrane via a novel pathway. , 1995, The EMBO journal.

[14]  T. Lithgow,et al.  Mas37p, a novel receptor subunit for protein import into mitochondria , 1995, The Journal of cell biology.

[15]  V. Braun,et al.  Specific phosphatidylethanolamine dependence of Serratia marcescens cytotoxin activity , 1997, Molecular microbiology.

[16]  T. Silhavy,et al.  Imp/OstA is required for cell envelope biogenesis in Escherichia coli , 2002, Molecular microbiology.

[17]  V. Braun,et al.  Molecular characterization of the hemolysin determinant of Serratia marcescens , 1988, Journal of bacteriology.

[18]  W. Schliebs,et al.  Peroxisomal matrix protein import: the transient pore model , 2005, Nature Reviews Molecular Cell Biology.

[19]  T. Rapoport,et al.  Protein translocation by the Sec61/SecY channel. , 2005, Annual review of cell and developmental biology.

[20]  Kentaro Inoue,et al.  The chloroplastic protein translocation channel Toc75 and its paralog OEP80 represent two distinct protein families and are targeted to the chloroplastic outer envelope by different mechanisms. , 2004, The Plant journal : for cell and molecular biology.

[21]  T. Becker,et al.  Prediction of the plant β‐barrel proteome: A case study of the chloroplast outer envelope , 2003, Protein science : a publication of the Protein Society.

[22]  J. Tommassen,et al.  Identification of an outer membrane protein required for the transport of lipopolysaccharide to the bacterial cell surface. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[23]  J. Massagué,et al.  Nucleocytoplasmic shuttling of signal transducers , 2004, Nature Reviews Molecular Cell Biology.

[24]  D. Stojanovski,et al.  Dissection of the Mitochondrial Import and Assembly Pathway for Human Tom40* , 2005, Journal of Biological Chemistry.

[25]  D. Mokranjac,et al.  Tob38, a novel essential component in the biogenesis of β‐barrel proteins of mitochondria , 2004, EMBO reports.

[26]  E. Willery,et al.  Lack of functional complementation between Bordetella pertussis filamentous hemagglutinin and Proteus mirabilis HpmA hemolysin secretion machineries , 1997, Journal of bacteriology.

[27]  K. Keegstra,et al.  The evolutionary origin of the protein-translocating channel of chloroplastic envelope membranes: identification of a cyanobacterial homolog. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[28]  Characterization of six lipoproteins in the sigmaE regulon. , 2005, Journal of bacteriology.

[29]  G. Schulz.  β-Barrel membrane proteins , 2000 .

[30]  Trevor Lithgow,et al.  Assembling the mitochondrial outer membrane , 2004, Nature Structural &Molecular Biology.

[31]  J. W. Campbell,et al.  Experimental Determination and System Level Analysis of Essential Genes in Escherichia coli MG1655 , 2003, Journal of bacteriology.

[32]  I. Collinson,et al.  The protein translocation apparatus of chloroplast envelopes , 1998 .

[33]  J. Tommassen,et al.  Folding of a bacterial outer membrane protein during passage through the periplasm , 1997, The EMBO journal.

[34]  T. Endo,et al.  Two novel proteins in the mitochondrial outer membrane mediate β-barrel protein assembly , 2004, The Journal of cell biology.

[35]  B. Dobberstein,et al.  Common Principles of Protein Translocation Across Membranes , 1996, Science.

[36]  C. Gross,et al.  SurA, a periplasmic protein with peptidyl-prolyl isomerase activity, participates in the assembly of outer membrane porins. , 1996, Genes & development.

[37]  Daniel Kahne,et al.  Identification of a Multicomponent Complex Required for Outer Membrane Biogenesis in Escherichia coli , 2005, Cell.

[38]  Huilin Li,et al.  Evidence for conservation of architecture and physical properties of Omp85-like proteins throughout evolution. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[39]  C. Locht,et al.  Two‐partner secretion in Gram‐negative bacteria: a thrifty, specific pathway for large virulence proteins , 2001, Molecular microbiology.

[40]  A. Bolhuis,et al.  Protein targeting by the twin-arginine translocation pathway , 2001, Nature Reviews Molecular Cell Biology.

[41]  E. Willery,et al.  Evidence that a globular conformation is not compatible with FhaC‐mediated secretion of the Bordetella pertussis filamentous haemagglutinin , 1998, Molecular microbiology.

[42]  M. Yaffe,et al.  Regulation of mitochondrial morphology and inheritance by Mdm10p, a protein of the mitochondrial outer membrane , 1994, The Journal of cell biology.

[43]  Christiane Lohaus,et al.  The mitochondrial morphology protein Mdm10 functions in assembly of the preprotein translocase of the outer membrane. , 2004, Developmental cell.

[44]  N. Pfanner,et al.  An Essential Role of Sam50 in the Protein Sorting and Assembly Machinery of the Mitochondrial Outer Membrane* , 2003, Journal of Biological Chemistry.

[45]  T. Silhavy,et al.  Chemical Conditionality A GeneticStrategy to Probe Organelle Assembly , 2005, Cell.

[46]  A. Valencia,et al.  POTRA: a conserved domain in the FtsQ family and a class of beta-barrel outer membrane proteins. , 2003, Trends in biochemical sciences.

[47]  R. Waller,et al.  The Omp85 family of proteins is essential for outer membrane biogenesis in mitochondria and bacteria , 2004, The Journal of cell biology.

[48]  Kentaro Inoue,et al.  A Molecular-Genetic Study of the Arabidopsis Toc75 Gene Family1 , 2005, Plant Physiology.

[49]  P. Roholl,et al.  The Omp85 protein of Neisseria meningitidis is required for lipid export to the outer membrane , 2003, The EMBO journal.

[50]  J. Tommassen,et al.  Role of a Highly Conserved Bacterial Protein in Outer Membrane Protein Assembly , 2003, Science.

[51]  C. Raetz,et al.  Loss of Outer Membrane Proteins without Inhibition of Lipid Export in an Escherichia coli YaeT Mutant* , 2005, Journal of Biological Chemistry.

[52]  T. Silhavy,et al.  Genetic Evidence for Parallel Pathways of Chaperone Activity in the Periplasm of Escherichia coli , 2001, Journal of bacteriology.

[53]  M. Colombini,et al.  Catalyzed insertion of proteins into phospholipid membranes: specificity of the process. , 2002, Biophysical journal.

[54]  F. Nargang,et al.  The Tim8-Tim13 Complex of Neurospora crassa Functions in the Assembly of Proteins into Both Mitochondrial Membranes* , 2004, Journal of Biological Chemistry.

[55]  Sabine Cornelsen,et al.  Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[56]  T. Becker,et al.  The Evolutionarily Related β-Barrel Polypeptide Transporters from Pisum sativum and Nostoc PCC7120 Contain Two Distinct Functional Domains* , 2005, Journal of Biological Chemistry.

[57]  N. Pfanner,et al.  Biogenesis of the Protein Import Channel Tom40 of the Mitochondrial Outer Membrane , 2004, Journal of Biological Chemistry.

[58]  E. Schleiff,et al.  A Toc75‐like protein import channel is abundant in chloroplasts , 2002, EMBO reports.

[59]  B. Bukau,et al.  Toc12, a novel subunit of the intermembrane space preprotein translocon of chloroplasts. , 2004, Molecular biology of the cell.

[60]  N. Pfanner,et al.  Sam35 of the Mitochondrial Protein Sorting and Assembly Machinery Is a Peripheral Outer Membrane Protein Essential for Cell Viability* , 2004, Journal of Biological Chemistry.