In the last decade, there has been an explosion of publications on the assembly of β-barrel outer membrane proteins (OMPs), which carry out diverse cellular functions, including solute transport, protein secretion, and assembly of protein and lipid components of the outer membrane. Of the three outer membrane model systems—Gram-negative bacteria, mitochondria and chloroplasts—research on bacterial and mitochondrial systems has so far led the way in dissecting the β-barrel OMP assembly pathways. Many exciting discoveries have been made, including the identification of β-barrel OMP assembly machineries in bacteria and mitochondria, and potentially the core assembly component in chloroplasts. The atomic structures of all five components of the bacterial β-barrel assembly machinery (BAM) complex, except the β-barrel domain of the core BamA protein, have been solved. Structures reveal that these proteins contain domains/motifs known to facilitate protein-protein interactions, which are at the heart of the assembly pathways. While structural information has been valuable, most of our current understanding of the β-barrel OMP assembly pathways has come from genetic, molecular biology, and biochemical analyses. This paper provides a comparative account of the β-barrel OMP assembly pathways in Gram-negative bacteria, mitochondria, and chloroplasts. 1. Introduction The outer membrane encircles Gram-negative bacteria, mitochondria, and chloroplasts. Embedded within this membrane is a unique class of proteins that fold into a β-barrel structure consisting of 8 to 22 antiparallel β-strands, interacting through hydrogen bonding to the neighboring strands, with the first strand being frequently hydrogen bonded to the last strand. Atomic structures of an impressive number of the β-barrel outer membrane proteins (OMPs) have been solved [1]. In general, the nonpolar side chains of a folded β-barrel are oriented outwardly towards the lipid bilayer of the membrane, while the polar side chains are exposed inwardly towards the interior of the barrel that often forms a channel. The two main activities of the β-barrel OMPs are to permit transport/insertion of proteins and diffusion of solutes across the outer membrane. The latter class of proteins is called porin [2]. These fundamental activities make the outer membrane an immensely important cellular structure of Gram-negative bacteria and eukaryotes. In Gram-negative bacteria, the assembly and insertion of porin and non-porin proteins are catalyzed by the β-barrel assembly machinery (BAM) [3–6]. The BAM complex also assists
References
[1]
J. W. Fairman, N. Noinaj, and S. K. Buchanan, “The structural biology of β-barrel membrane proteins: a summary of recent reports,” Current Opinion in Structural Biology, vol. 21, no. 4, pp. 523–531, 2011.
[2]
T. Nakae, “Identification of the outer membrane protein of E. coli that produces transmembrane channels in reconstituted vesicle membranes,” Biochemical and Biophysical Research Communications, vol. 71, no. 3, pp. 877–884, 1976.
[3]
R. Misra, “First glimpse of the crystal structure of YaeT's POTRA domains,” American Chemical Society Chemical Biology, vol. 2, no. 10, pp. 649–651, 2007.
[4]
C. L. Hagan, T. J. Silhavy, and D. Kahne, “β-barrel membrane protein assembly by the bam complex,” Annual Review of Biochemistry, vol. 80, no. 1, pp. 189–210, 2011.
[5]
D. P. Ricci and T. J. Silhavy, “The Bam machine: a molecular cooper,” Biochimica et Biophysica Acta, vol. 1818, no. 4, pp. 1067–1084, 2012.
[6]
K. H. Kim, S. Aulakh, and M. Paetzel, “The bacterial outer membrane β-barrel assembly machinery,” Protein Science, vol. 21, no. 6, pp. 751–768, 2012.
[7]
M. P. Bos, B. Tefsen, J. Geurtsen, and J. Tommassen, “Identification of an outer membrane protein required for the transport of lipopolysaccharide to the bacterial cell surface,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 25, pp. 9417–9422, 2004.
[8]
D. Bennion, E. S. Charlson, E. Coon, and R. Misra, “Dissection of β-barrel outer membrane protein assembly pathways through characterizing BamA POTRA 1 mutants of Escherichia coli,” Molecular Microbiology, vol. 77, no. 5, pp. 1153–1171, 2010.
[9]
R. Ieva and H. D. Bernstein, “Interaction of an autotransporter passenger domain with BamA during its translocation across the bacterial outer membrane,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 45, pp. 19120–19125, 2009.
[10]
O. Schmidt, N. Pfanner, and C. Meisinger, “Mitochondrial protein import: from proteomics to functional mechanisms,” Nature Reviews Molecular Cell Biology, vol. 11, no. 9, pp. 655–667, 2010.
[11]
C. Andrès, B. Agne, and F. Kessler, “The TOC complex: preprotein gateway to the chloroplast,” Biochimica et Biophysica Acta, vol. 1803, no. 6, pp. 715–723, 2010.
[12]
N. Pfanner, N. Wiedemann, C. Meisinger, and T. Lithgow, “Assembling the mitochondrial outer membrane,” Nature Structural and Molecular Biology, vol. 11, no. 11, pp. 1044–1048, 2004.
[13]
D. M. Walther, D. Rapaport, and J. Tommassen, “Biogenesis of β-barrel membrane proteins in bacteria and eukaryotes: evolutionary conservation and divergence,” Cellular and Molecular Life Sciences, vol. 66, no. 17, pp. 2789–2804, 2009.
[14]
S. C. Hsu and K. Inoue, “Two evolutionarily conserved essential β-barrel proteins in the chloroplast outer envelope membrane,” Bioscience Trends, vol. 3, no. 5, pp. 168–178, 2009.
[15]
T. Cavalier-Smith, “Origin of mitochondria by intracellular enslavement of a photosynthetic purple bacterium,” Proceedings of Royal Society Biological Sciences, vol. 273, no. 1596, pp. 1943–1952, 2006.
[16]
J. M. Archibald, “The puzzle of plastid esvolution,” Current Biology, vol. 19, no. 2, pp. R81–R88, 2009.
[17]
J. H. Jiang, J. Tong, K. S. Tan, and K. Gabriel, “From evolution to pathogenesis: the link between β-barrel assembly machineries in the outer membrane of mitochondria and Gram-negative bacteria,” International Journal of Molecular Sciences, vol. 13, no. 7, pp. 8038–8050, 2012.
[18]
K. Eckart, L. Eichacker, K. Sohrt, E. Schleiff, L. Heins, and J. Soll, “A Toc75-like protein import channel is abundant in chloroplasts,” European Molecular Biology Organization Reports, vol. 3, no. 6, pp. 557–562, 2002.
[19]
V. Kozjak, N. Wiedemann, D. Milenkovic et al., “An essential role of Sam50 in the protein sorting and assembly machinery of the mitochondrial outer membrane,” Journal of Biological Chemistry, vol. 278, no. 49, pp. 48520–48523, 2003.
[20]
S. A. Paschen, T. Waizenegger, T. Stan et al., “Evolutionary conservation of biogenesis of β-barrel membrane proteins,” Nature, vol. 426, no. 6968, pp. 862–866, 2003.
[21]
R. Voulhoux, M. P. Bos, J. Geurtsen, M. Mols, and J. Tommassen, “Role of a highly conserved bacterial protein in outer membrane protein assembly,” Science, vol. 299, no. 5604, pp. 262–265, 2003.
[22]
I. Gentle, K. Gabriel, P. Beech, R. Waller, and T. Lithgow, “The Omp85 family of proteins is essential for outer membrane biogenesis in mitochondria and bacteria,” Journal of Cell Biology, vol. 164, no. 1, pp. 19–24, 2004.
[23]
K. Inoue and D. Potter, “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,” The Plant Journal, vol. 39, no. 3, pp. 354–365, 2004.
[24]
T. Wu, J. Malinverni, N. Ruiz, S. Kim, T. J. Silhavy, and D. Kahne, “Identification of a multicomponent complex required for outer membrane biogenesis in Escherichia coli,” Cell, vol. 121, no. 2, pp. 235–245, 2005.
[25]
B. B？lter, J. Soll, A. Schulz, S. Hinnah, and R. Wagner, “Origin of a chloroplast protein importer,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 26, pp. 15831–15836, 1998.
[26]
S. Reumann, J. Davila-Aponte, and K. Keegstra, “The evolutionary origin of the protein-translocating channel of chloroplastic envelope membranes: identification of a cyanobacterial homolog,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 2, pp. 784–789, 1999.
[27]
R. Patel, S. C. Hsu, J. Bédard, K. Inoue, and P. Jarvis, “The Omp85-related chloroplast outer envelope protein OEP80 is essential for viability in Arabidopsis,” Plant Physiology, vol. 148, no. 1, pp. 235–245, 2008.
[28]
B. A. Sampson, R. Misra, and S. A. Benson, “Identification and characterization of a new gene of Escherichia coli K-12 involved in outer membrane permeability,” Genetics, vol. 122, no. 3, pp. 491–501, 1989.
[29]
U. S. Eggert, N. Ruiz, B. V. Falcone et al., “Genetic basis for activity differences between vancomycin and glycolipid derivatives of vancomycin,” Science, vol. 294, no. 5541, pp. 361–364, 2001.
[30]
J. G. Sklar, T. Wu, L. S. Gronenberg, J. C. Malinverni, D. Kahne, and T. J. Silhavy, “Lipoprotein SmpA is a component of the YaeT complex that assembles outer membrane proteins in Escherichia coli,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 15, pp. 6400–6405, 2007.
[31]
M. Braun and T. J. Silhavy, “Imp/OstA is required for cell envelope biogenesis in Escherichia coli,” Molecular Microbiology, vol. 45, no. 5, pp. 1289–1302, 2002.
[32]
N. Ruiz, D. Kahne, and T. J. Silhavy, “Transport of lipopolysaccharide across the cell envelope: the long road of discovery,” Nature Reviews Microbiology, vol. 7, no. 9, pp. 677–683, 2009.
[33]
S. M. Galloway and C. R. H. Raetz, “A mutant of Escherichia coli defective in the first step of endotoxin biosynthesis,” Journal of Biological Chemistry, vol. 265, no. 11, pp. 6394–6402, 1990.
[34]
L. Steeghs, R. den Hartog, A. den Boer, B. Zomer, P. Roholl, and P. van der Ley, “Meningitis bacterium is viable without endotoxin,” Nature, vol. 392, no. 6675, pp. 449–450, 1998.
[35]
R. Tellez Jr. and R. Misra, “Substitutions in the BamA β-barrel domain overcome the conditional lethal phenotype of a strain of Escherichia coli,” Journal of Bacteriology, vol. 194, no. 2, pp. 317–324, 2012.
[36]
K. Anwari, C. T. Webb, S. Poggio et al., “The evolution of new lipoprotein subunits of the bacterial outer membrane BAM complex,” Molecular Microbiology, vol. 84, no. 5, pp. 832–844, 2012.
[37]
W. T. Doerrler and C. R. H. Raetz, “Loss of outer membrane proteins without inhibition of lipid export in an Escherichia coli YaeT mutant,” Journal of Biological Chemistry, vol. 280, no. 30, pp. 27679–27687, 2005.
[38]
J. Werner and R. Misra, “YaeT (Omp85) affects the assembly of lipid-dependent and lipid-independent outer membrane proteins of Escherichia coli,” Molecular Microbiology, vol. 57, no. 5, pp. 1450–1459, 2005.
[39]
J. C. Malinverni, J. Werner, S. Kim et al., “YfiO stabilizes the YaeT complex and is essential for outer membrane protein assembly in Escherichia coli,” Molecular Microbiology, vol. 61, no. 1, pp. 151–164, 2006.
[40]
E. B. Volokhina, F. Beckers, J. Tommassen, and M. P. Bos, “The β-barrel outer membrane protein assembly complex of Neisseria meningitidis,” Journal of Bacteriology, vol. 191, no. 22, pp. 7074–7085, 2009.
[41]
C. T. Webb, E. Heinz, and T. Lithgow, “Evolution of the β-barrel assembly machinery,” Trends in Microbiology. In press.
[42]
S. Gratzer, T. Lithgow, R. E. Bauer et al., “Mas37p, a novel receptor subunit for protein import into mitochondria,” Journal of Cell Biology, vol. 129, no. 1, pp. 25–34, 1995.
[43]
N. Pfanner and M. Meijer, “Mitochondrial biogenesis: the Tom and Tim machine,” Current Biology, vol. 7, no. 2, pp. R100–R103, 1997.
[44]
M. T. Ryan, H. Müller, and N. Pfanner, “Functional staging of ADP/ATP carrier translocation across the outer mitochondrial membrane,” Journal of Biological Chemistry, vol. 274, no. 29, pp. 20619–20627, 1999.
[45]
N. Wiedemann, V. Kozjak, A. Chacinska et al., “Machinery for protein sorting and assembly in the mitochondrial outer membrane,” Nature, vol. 424, no. 6948, pp. 565–571, 2003.
[46]
D. Milenkovic, V. Kozjak, N. Wiedemann et al., “Sam35 of the mitochondrial protein sorting and assembly machinery is a peripheral outer membrane protein essential for cell viability,” Journal of Biological Chemistry, vol. 279, no. 21, pp. 22781–22785, 2004.
[47]
T. Waizenegger, S. J. Habib, M. Lech et al., “Tob38, a novel essential component in the biogenesis of β-barrel proteins of mitochondria,” European Molecular Biology Organization Reports, vol. 5, no. 7, pp. 704–709, 2004.
[48]
D. Ishikawa, H. Yamamoto, Y. Tamura, K. Moritoh, and T. Endo, “Two novel proteins in the mitochondrial outer membrane mediate β-barrel protein assembly,” Journal of Cell Biology, vol. 166, no. 5, pp. 621–627, 2004.
[49]
C. Meisinger, M. Rissler, A. Chacinska et al., “The mitochondrial morphology protein Mdm10 functions in assembly of the preprotein translocase of the outer membrane,” Developmental Cell, vol. 7, no. 1, pp. 61–71, 2004.
[50]
L. F. Sogo and M. P. Yaffe, “Regulation of mitochondrial morphology and inheritance by Mdm10p, a protein of the mitochondrial outer membrane,” Journal of Cell Biology, vol. 126, no. 6, pp. 1361–1373, 1994.
[51]
L. Sánchez-Pulido, D. Devos, S. Genevrois, M. Vicente, and A. Valencia, “POTRA: a conserved domain in the FtsQ family and a class of β-barrel outer membrane proteins,” Trends in Biochemical Sciences, vol. 28, no. 10, pp. 523–526, 2003.
[52]
S. Moslavac, O. Mirus, R. Bredemeier, J. Soll, A. von Haeseler, and E. Schleiff, “Conserved pore-forming regions in polypeptide-transporting proteins,” FEBS Journal, vol. 272, no. 6, pp. 1367–1378, 2005.
[53]
I. E. Gentle, L. Burri, and T. Lithgow, “Molecular architecture and function of the Omp85 family of proteins,” Molecular Microbiology, vol. 58, no. 5, pp. 1216–1225, 2005.
[54]
F. Jacob-Dubuisson, V. Villeret, B. Clantin, A. S. Delattre, and N. Saint, “First structural insights into the TpsB/Omp85 superfamily,” Biological Chemistry, vol. 390, no. 8, pp. 675–684, 2009.
[55]
B. Clantin, A. S. Delattre, P. Rucktooa et al., “Structure of the membrane protein FhaC: a member of the Omp85-TpsB transporter superfamily,” Science, vol. 317, no. 5840, pp. 957–961, 2007.
[56]
A. S. Delattre, B. Clantin, N. Saint, C. Locht, V. Villeret, and F. Jacob-Dubuisson, “Functional importance of a conserved sequence motif in FhaC, a prototypic member of the TpsB/Omp85 superfamily,” FEBS Journal, vol. 277, no. 22, pp. 4755–4765, 2010.
[57]
M. Leonard-Rivera and R. Misra, “Conserved residues of the putative L6 loop of Escherichia coli BamA play a critical role in the assembly of β-barrel outer membrane proteins, including that of BamA itself,” Journal of Bacteriology, vol. 194, no. 17, pp. 4662–4668, 2012.
[58]
J. F. Stegmeier and C. Andersen, “Characterization of pores formed by YaeT (Omp85) from Escherichia coli,” Journal of Biochemistry, vol. 140, no. 2, pp. 275–283, 2006.
[59]
V. Robert, E. B. Volokhina, F. Senf, M. P. Bos, P. van Gelder, and J. Tommassen, “Assembly factor Omp85 recognizes its outer membrane protein substrates by a species-specific C-terminal motif,” PLoS Biology, vol. 4, no. 11, pp. 1984–1995, 2006.
[60]
R. Bredemeier, T. Schlegel, F. Ertel et al., “Functional and phylogenetic properties of the pore-forming β-barrel transporters of the Omp85 family,” Journal of Biological Chemistry, vol. 282, no. 3, pp. 1882–1890, 2007.
[61]
S. Kutik, D. Stojanovski, L. Becker et al., “Dissecting membrane insertion ofmitochondrial β-barrel proteins,” Cell, vol. 132, no. 6, pp. 1011–1024, 2008.
[62]
J. Nesper, A. Brosig, P. Ringler et al., “Omp from Thermus thermophilus HB27: an ancestral type of the Omp85 protein family,” Journal of Bacteriology, vol. 190, no. 13, pp. 4568–4575, 2008.
[63]
T. Arnold, K. Zeth, and D. Linke, “Omp85 from the thermophilic cyanobacterium Thermosynechococcus elongatus differs from proteobacterial Omp85 in structure and domain composition,” Journal of Biological Chemistry, vol. 285, no. 23, pp. 18003–18015, 2010.
[64]
U. Ahting, M. Thieffry, H. Engelhardt, R. Hegerl, W. Neupert, and S. Nussberger, “Tom40, the pore-forming component of the protein-conducting TOM channel in the outer membrane of mitochondria,” Journal of Cell Biology, vol. 153, no. 6, pp. 1151–1160, 2001.
[65]
S. Kim, J. C. Malinverni, P. Sliz, T. J. Silhavy, S. C. Harrison, and D. Kahne, “Structure and function of an essential component of the outer membrane protein assembly machine,” Science, vol. 317, no. 5840, pp. 961–964, 2007.
[66]
M. P. Bos, V. Robert, and J. Tommassen, “Functioning of outer membrane protein assembly factor Omp85 requires a single POTRA domain,” European Molecular Biology Organization Reports, vol. 8, no. 12, pp. 1149–1154, 2007.
[67]
E. B. Volokhina, J. Grijpstra, M. Stork, I. Schilders, J. Tommassen, and M. P. Bos, “Role of the periplasmic chaperones Skp, SurA, and DegQ in outer membrane protein biogenesis in Neisseria meningitidis,” Journal of Bacteriology, vol. 193, no. 7, pp. 1612–1621, 2011.
[68]
G. Ried, I. Hindennach, and U. Henning, “Role of lipopolysaccharide in assembly of Escherichia coli outer membrane proteins OmpA, OmpC, and OmpF,” Journal of Bacteriology, vol. 172, no. 10, pp. 6048–6053, 1990.
[69]
M. W. Laird, A. W. Kloser, and R. Misra, “Assembly of LamB and OmpF in deep rough lipopolysaccharide mutants of Escherichia coli K-12,” Journal of Bacteriology, vol. 176, no. 8, pp. 2259–2264, 1994.
[70]
S. J. Habib, T. Waizenegger, A. Niewienda, S. A. Paschen, W. Neupert, and D. Rapaport, “The N-terminal domain of Tob55 has a receptor-like function in the biogenesis of mitochondrial β-barrel proteins,” Journal of Cell Biology, vol. 176, no. 1, pp. 77–88, 2007.
[71]
W. C. Wimley, “The versatile β-barrel membrane protein,” Current Opinion in Structural Biology, vol. 13, no. 4, pp. 404–411, 2003.
[72]
M. Remmert, D. Linke, A. N. Lupas, and J. S？ding, “HHomp—prediction and classification of outer membrane proteins,” Nucleic Acids Research, vol. 37, no. 2, pp. W446–W451, 2009.
[73]
P. Koenig, O. Mirus, R. Haarmann et al., “Conserved properties of polypeptide transport-associated (POTRA) domains derived from cyanobacterial Omp85,” Journal of Biological Chemistry, vol. 285, no. 23, pp. 18016–18024, 2010.
[74]
N. Ruiz, B. Falcone, D. Kahne, and T. J. Silhavy, “Chemical conditionality: a genetic strategy to probe organelle assembly,” Cell, vol. 121, no. 2, pp. 307–317, 2005.
[75]
E. S. Charlson, J. N. Werner, and R. Misra, “Differential effects of yfgL mutation on Escherichia coli outer membrane proteins and lipopolysaccharide,” Journal of Bacteriology, vol. 188, no. 20, pp. 7186–7194, 2006.
[76]
P. Workman, K. Heide, N. Giuliano, et al., “Genetic, biochemical, and molecular characterization of the polypeptide transport-associated domain of Escherichia coli BamA,” Journal of Bacteriology, vol. 194, no. 13, pp. 3512–3521, 2012.
[77]
D. Vertommen, N. Ruiz, P. Leverrier, T. J. Silhavy, and J. F. Collet, “Characterization of the role of the Escherichia coli periplasmic chaperone SurA using differential proteomics,” Proteomics, vol. 9, no. 9, pp. 2432–2443, 2009.
[78]
T. J. Knowles, M. Jeeves, S. Bobat et al., “Fold and function of polypeptide transport-associated domains responsible for delivering unfolded proteins to membranes,” Molecular Microbiology, vol. 68, no. 5, pp. 1216–1227, 2008.
[79]
D. A. Stroud, T. Becker, J. Qiu, et al., “Biogenesisof mitochondrial β-barrel proteins: the POTRA domain is involved in precursor release from the SAM complex,” Molecular Biology of the Cell, vol. 22, no. 16, pp. 2823–2833, 2011.
[80]
M. S. Sommer, B. Daum, L. E. Gross et al., “Chloroplast Omp85 proteins change orientation during evolution,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 33, pp. 13841–13846, 2011.
[81]
C. T. Webb, J. Selkrig, A. J. Perry, N. Noinaj, S. K. Buchanan, and T. Lithgow, “Dynamic association of BAM complex modules includes surface exposure of the lipoprotein BamC,” Journal of Molecular Biology, vol. 422, no. 4, pp. 545–555, 2012.
[82]
M. Fussenegger, D. Facius, J. Meier, and T. F. Meyer, “A novel peptidoglycan-linked lipoprotein (ComL) that functions in natural transformation competence of Neisseria gonorrhoeae,” Molecular Microbiology, vol. 19, no. 5, pp. 1095–1105, 1996.
[83]
C. Onufryk, M. L. Crouch, F. C. Fang, and C. A. Gross, “Characterization of six lipoproteins in the σe regulon,” Journal of Bacteriology, vol. 187, no. 13, pp. 4552–4561, 2005.
[84]
N. W. Rigel, J. Schwalm, D. P. Ricci, and T. J. Silhavy, “BamE modulates the Escherichia coliβ-barrel assembly machine component BamA,” Journal of Bacteriology, vol. 194, no. 5, pp. 1002–1008, 2012.
[85]
C. M. Sandoval, S. L. Baker, K. Jansen, S. I. Metzner, and M. C. Sousa, “Crystal structure of BamD: an essential component of the β-barrel assembly machinery of gram-negative bacteria,” Journal of Molecular Biology, vol. 409, no. 3, pp. 348–357, 2011.
[86]
C. Dong, H. F. Hou, X. Yang, Y. Q. Shen, and Y. H. Dong, “Structure of Escherichia coli BamD and its functional implications in outer membrane protein assembly,” Acta Crystallography, vol. 68, no. 2, pp. 95–101, 2012.
[87]
R. Albrecht and K. Zeth, “Structural basis of outer membrane protein biogenesis in bacteria,” Journal of Biological Chemistry, vol. 286, no. 31, pp. 27792–27803, 2011.
[88]
L. D. D'Andrea and L. Regan, “TPR proteins: the versatile helix,” Trends in Biochemical Sciences, vol. 28, no. 12, pp. 655–662, 2003.
[89]
K. H. Kim, S. Aulakh, and M. Paetzel, “Crystal structure of β-barrel assembly machinery BamCD protein complex,” Journal of Biological Chemistry, vol. 286, no. 45, pp. 39116–39121, 2011.
[90]
C. L. Hagan, S. Kim, and D. Kahne, “Reconstitution of outer membrane protein assembly from purified components,” Science, vol. 328, no. 5980, pp. 890–892, 2010.
[91]
D. P. Ricci, C. L. Hagan, D. Kahne, and T. J. Silhavy, “Activation of the Escherichia coliβ-barrel assembly machine (Bam) is required for essential components to interact properly with substrate,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 9, pp. 3487–3491, 2012.
[92]
P. Vuong, D. Bennion, J. Mantei, D. Frost, and R. Misra, “Analysis of YfgL and YaeT interactions through bioinformatics, mutagenesis, and biochemistry,” Journal of Bacteriology, vol. 190, no. 5, pp. 1507–1517, 2008.
[93]
A. Heuck, A. Schleiffer, and T. Clausen, “Augmenting β-augmentation: structural basis of how BamB binds BamA and may support folding of outer membrane proteins,” Journal of Molecular Biology, vol. 406, no. 5, pp. 659–666, 2011.
[94]
K. H. Kim and M. Paetzel, “Crystal structure of Escherichia coli BamB, a lipoprotein component of the β-barrel assembly machinery complex,” Journal of Molecular Biology, vol. 406, no. 5, pp. 667–678, 2011.
[95]
N. Noinaj, J. W. Fairman, and S. K. Buchanan, “The crystal structure of BamB suggests interactions with BamA and its role within the BAM complex,” Journal of Molecular Biology, vol. 407, no. 2, pp. 248–260, 2011.
[96]
T. J. Knowles, D. F. Browning, M. Jeeves et al., “Structure and function of BamE within the outer membrane and the β-barrel assembly machine,” European Molecular Biology Organization Reports, vol. 12, no. 2, pp. 123–128, 2011.
[97]
C. U. Stirnimann, E. Petsalaki, R. B. Russell, and C. W. Müller, “WD40 proteins propel cellular networks,” Trends in Biochemical Sciences, vol. 35, no. 10, pp. 565–574, 2010.
[98]
P. Z. Gatzeva-Topalova, T. A. Walton, and M. C. Sousa, “Crystal structure of YaeT: conformational flexibility and substrate recognition,” Structure, vol. 16, no. 12, pp. 1873–1881, 2008.
[99]
C. L. Hagan and D. Kahne, “The reconstitution of Escherichia coli Bam complex catalyzes multiple rounds of β-barrel assembly,” Biochemistry, vol. 50, no. 35, pp. 7444–7446, 2011.
[100]
R. Niedenthal, L. Riles, U. Güldener, S. Klein, M. Johnston, and J. H. Hegemann, “Systematic analysis of S. cerevisiae chromosome VIII genes,” Yeast, vol. 15, no. 16, pp. 1775–1796, 1999.
[101]
N. C. Chan and T. Lithgow, “The peripheral membrane subunits of the SAM complex function codependently in mitochondrial outer membrane biogenesis,” Molecular Biology of the Cell, vol. 19, no. 1, pp. 126–136, 2008.
[102]
N. Wiedemann, K. N. Truscott, S. Pfannschmidt, B. Guiard, C. Meisinger, and N. Pfanner, “Biogenesis of the protein import channel Tom40 of the mitochondrial outer membrane: Intermembrane space components are involved in an early stage of the assembly pathway,” Journal of Biological Chemistry, vol. 279, no. 18, pp. 18188–18194, 2004.
[103]
K. Model, C. Meisinger, T. Prinz et al., “Multistep assembly of the protein import channel of the mitochondrial outer membrane,” Nature Structural Biology, vol. 8, no. 4, pp. 361–370, 2001.
[104]
B. Kornmann, E. Currie, S. R. Collins et al., “An ER-mitochondria tethering complex revealed by a synthetic biology screen,” Science, vol. 325, no. 5939, pp. 477–481, 2009.
[105]
K. Yamano, S. Tanaka-Yamano, and T. Endo, “Mdm10 as a dynamic constituent of the TOB/SAM complex directs coordinated assembly of Tom40,” European Molecular Biology Organization Reports, vol. 11, no. 3, pp. 187–193, 2010.
[106]
A. Kouranov, X. Chen, B. Fuks, and D. J. Schnell, “Tic20 and Tic22 are new components of the protein import apparatus at the chloroplast inner envelope membrane,” Journal of Cell Biology, vol. 143, no. 4, pp. 991–1002, 1998.
[107]
J. Tripp, A. Hahn, P. Koenig et al., “Structure and conservation of the periplasmic targeting factor Tic22 protein from plants and cyanobacteria,” Journal of Biological Chemistry, vol. 287, no. 29, pp. 24164–24173, 2012.
[108]
S. W. Lazar and R. Kolter, “SurA assists the folding of Escherichia coli outer membrane proteins,” Journal of Bacteriology, vol. 178, no. 6, pp. 1770–1773, 1996.
[109]
P. E. Rouvière and C. A. Gross, “SurA, a periplasmic protein with peptidyl-prolyl isomerase activity, participates in the assembly of outer membrane porins,” Genes and Development, vol. 10, no. 24, pp. 3170–3182, 1996.
[110]
J. G. Sklar, T. Wu, D. Kahne, and T. J. Silhavy, “Defining the roles of the periplasmic chaperones SurA, Skp, and DegP in Escherichia coli,” Genes and Development, vol. 21, no. 19, pp. 2473–2484, 2007.
[111]
S. Behrens-Kneip, “The role of SurA factor in outer membrane protein transport and virulence,” International Journal of Medical Microbiology, vol. 300, no. 7, pp. 421–428, 2010.
[112]
J. Werner, A. M. Augustus, and R. Misra, “Assembly of TolC, a structurally unique and multifunctional outer membrane protein of Escherichia coli K-12,” Journal of Bacteriology, vol. 185, no. 22, pp. 6540–6547, 2003.
[113]
M. Masi, G. Duret, A. H. Delcour, and R. Misra, “Folding and trimerization of signal sequence-less mature TolC in the cytoplasm of Escherichia coli,” Microbiology, vol. 155, no. 6, pp. 1847–1857, 2009.
[114]
N. Bolender, A. Sickmann, R. Wagner, C. Meisinger, and N. Pfanner, “Multiple pathways for sorting mitochondrial precursor proteins,” European Molecular Biology Organization Reports, vol. 9, no. 1, pp. 42–49, 2008.
[115]
H. Remaut and G. Waksman, “Protein-protein interaction through β-strand addition,” Trends in Biochemical Sciences, vol. 31, no. 8, pp. 436–444, 2006.
[116]
A. R. Ureta, R. G. Endres, N. S. Wingreen, and T. J. Silhavy, “Kinetic analysis of the assembly of the outer membrane protein LamB in Escherichia coli mutants each lacking a secretion or targeting factor in a different cellular compartment,” Journal of Bacteriology, vol. 189, no. 2, pp. 446–454, 2007.
[117]
T. Ulrich, L. E. Gross, M. S. Sommer, E. Schleiff, and D. Rapaport, “Chloroplast β-barrel proteins are assembled into the mitochondrial outer membrane in a process that depends on the TOM and TOB complexes,” Journal of Biological Chemistry, vol. 287, no. 33, pp. 27467–27479, 2012.
[118]
D. Stojanovski, B. Guiard, V. Kozjak-Pavlovic, N. Pfanner, and C. Meisinger, “Alternative function for the mitochondrial SAM complex in biogenesis of α-helical TOM proteins,” Journal of Cell Biology, vol. 179, no. 5, pp. 881–893, 2007.
[119]
L. K. Tamm, H. Hong, and B. Liang, “Folding and assembly of β-barrel membrane proteins,” Biochimica et Biophysica Acta, vol. 1666, no. 1-2, pp. 250–263, 2004.
