Outer membrane protein design

Current Opinion in Structural Biology

Volumn 45, Issue , 2017, Pages 45-52

  Slusky, Joanna SG ^a  

^a UNIVERSITY OF KANSAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OUTER MEMBRANE PROTEIN;

BACTERIAL OUTER MEMBRANE; BETA CHAIN; CHLOROPLAST; CONFORMATIONAL TRANSITION; GRAM NEGATIVE BACTERIUM; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; CHEMISTRY; GENETICS; METABOLISM; PROCEDURES; PROTEIN ENGINEERING;

BACTERIAL OUTER MEMBRANE PROTEINS; PROTEIN ENGINEERING;

EID: 84997822153     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2016.11.003     Document Type: Review

References (66)

1. 1 Hagan, C.L., Silhavy, T.J., Kahne, D., β-Barrel membrane protein assembly by the Bam complex. Annu Rev Biochem 80 (2011), 189–210.
2. 2 Osborne, A.R., Rapoport, T.A., van den Berg, B., Protein translocation by the Sec61/SecY channel. Annu Rev Cell Dev Biol 21 (2005), 529–550.
3. 3 Dong, C., Beis, K., Nesper, J., Brunkan-LaMontagne, A.L., Clarke, B.R., Whitfield, C., Naismith, J.H., Wza the translocon for E. coli capsular polysaccharides defines a new class of membrane protein. Nature 444 (2006), 226–229.
4. 4 Senes, A., Computational design of membrane proteins. Curr Opin Struct Biol 21 (2011), 460–466.
5. 5 Perez-Aguilar Jose, M., Saven Jeffery, G., Computational design of membrane proteins. Structure 20 (2012), 5–14.
6. 6 Ghirlanda, G., Design of membrane proteins: toward functional systems. Curr Opin Chem Biol 13 (2009), 643–651.
7. 7 Simms, J., Booth, P.J., Membrane proteins by accident or design. Curr Opin Chem Biol 17 (2013), 976–981.
8. 8 Scott, D.J., Kummer, L., Tremmel, D., Plückthun, A., Stabilizing membrane proteins through protein engineering. Curr Opin Chem Biol 17 (2013), 427–435.
9. 9 Ferguson, A.D., Hofmann, E., Coulton, J.W., Diederichs, K., Welte, W., Siderophore-mediated iron transport: crystal structure of FhuA with bound lipopolysaccharide. Science 282 (1998), 2215–2220.
10. 10 Yildiz, Ö., Vinothkumar, K.R., Goswami, P., Kühlbrandt, W., Structure of the monomeric outer-membrane porin OmpG in the open and closed conformation. EMBO J 25 (2006), 3702–3713.
11. 11 Cowan, S.W., Schirmer, T., Rummel, G., Steiert, M., Ghosh, R., Pauptit, R.A., Jansonius, J.N., Rosenbusch, J.P., Crystal structures explain functional properties of two E. coli porins. Nature 358 (1992), 727–733.
12. 12 Song, L., Hobaugh, M.R., Shustak, C., Cheley, S., Bayley, H., Gouaux, J.E., Structure of staphylococcal α-hemolysin, a heptameric transmembrane pore. Science 274 (1996), 1859–1865.
13. 13•• Koebnik, R., Krämer, L., Membrane assembly of circularly permuted variants of the E. coli outer membrane protein OmpA. J Mol Biol 250 (1995), 617–626 The authors divide OmpA's eight strands into hairpins and make OmpA variants of all possible orders of the hairpins. They find that only the circularly permuted variants fold and most of the circularly permuted variants retain the phage sensitivity phenotype.
14. 14 Cierpicki, T., Liang, B., Tamm, L.K., Bushweller, J.H., Increasing the accuracy of solution NMR structures of membrane proteins by application of residual dipolar couplings. High-resolution structure of outer membrane protein A. J Am Chem Soc 128 (2006), 6947–6951.
15. 15 Struyvé, M., Moons, M., Tommassen, J., Carboxy-terminal phenylalanine is essential for the correct assembly of a bacterial outer membrane protein. J Mol Biol 218 (1991), 141–148.
16. 16 Robert, V., Volokhina, E.B., Senf, F., Bos, M.P., Gelder, P.V., Tommassen, J., Assembly factor Omp85 recognizes its outer membrane protein substrates by a species-specific C-terminal motif. PLoS Biol, 4, 2006, e377.
17. 17 Koebnik, R., Structural and functional roles of the surface-exposed loops of the beta-barrel membrane protein OmpA from Escherichia coli. J Bacteriol 181 (1999), 3688–3694.
18. 18 Koebnik, R., Membrane assembly of the Escherichia coli outer membrane protein OmpA: exploring sequence constraints on transmembrane beta-strands. J Mol Biol 285 (1999), 1801–1810.
19. 19 Jimenez-Morales, D., Liang, J., Pattern of amino acid substitutions in transmembrane domains of β-barrel membrane proteins for detecting remote homologs in bacteria and mitochondria. PLoS ONE, 6, 2011, e26400.
20. 20 Cheley, S., Braha, O., Lu, X., Conlan, S., Bayley, H., A functional protein pore with a “retro” transmembrane domain. PRS 8 (1999), 1257–1267.
21. 21 Cheley, S., Malghani, M.S., Song, L., Hobaugh, M., Gouaux, J.E., Yang, J., Bayley, H., Spontaneous oligomerization of a staphylococcal alpha-hemolysin conformationally constrained by removal of residues that form the transmembrane beta-barrel. Protein Eng 10 (1997), 1433–1443.
22. 22•• Stapleton, J.A., Whitehead, T.A., Nanda, V., Computational redesign of the lipid-facing surface of the outer membrane protein OmpA. Proc Natl Acad Sci U S A 112 (2015), 9632–9637 The authors resurface the entirety of OmpA using a computational potential that encodes residue depth preference and sequence entropy. They find a series of cross back mutations that allow for OmpA folding and for the phage sensitivity phenotype.
23. 23 Hsieh, D., Davis, A., Nanda, V., A knowledge-based potential highlights unique features of membrane α-helical and β-barrel protein insertion and folding. Protein Sci 21 (2012), 50–62.
24. 24 Jackups, R. Jr., Liang, J., Interstrand pairing patterns in β-barrel membrane proteins: the positive-outside rule, aromatic rescue, and strand registration prediction. J Mol Biol 354 (2005), 979–993.
25. 25 Naveed, H., Jackups, R., Liang, J., Predicting weakly stable regions, oligomerization state, and protein–protein interfaces in transmembrane domains of outer membrane proteins. Proc Natl Acad Sci 106 (2009), 12735–12740.
26. 26 Naveed, H., Jimenez-Morales, D., Tian, J., Pasupuleti, V., Kenney, L.J., Liang, J., Engineered oligomerization state of OmpF protein through computational design decouples oligomer dissociation from unfolding. J Mol Biol 419 (2012), 89–101.
27. 27 Geula, S., Naveed, H., Liang, J., Shoshan-Barmatz, V., Structure-based analysis of VDAC1 protein: defining oligomer contact sites. J Biol Chem 287 (2012), 2179–2190.
28. 28 Gessmann, D., Mager, F., Naveed, H., Arnold, T., Weirich, S., Linke, D., Liang, J., Nussberger, S., Improving the resistance of a eukaryotic β-barrel protein to thermal and chemical perturbations. J Mol Biol 413 (2011), 150–161.
29. 29• Chen, M., Khalid, S., Sansom, M.S.P., Bayley, H., Outer membrane protein g: engineering a quiet pore for biosensing. Proc Natl Acad Sci U S A 105 (2008), 6272–6277 The authors stabilize the OmpG pore by deleting a bulge and cysteine crosslinking a loop. The resultant pore demonstrates very little gating.
30. 30 Grosse, W., Psakis, G., Mertins, B., Reiss, P., Windisch, D., Brademann, F., Bürck, J., Ulrich, A., Koert, U., Essen, L.-O., Structure-based engineering of a minimal porin reveals loop-independent channel closure. Biochemistry 53 (2014), 4826–4838.
31. 31 Mouritsen, O.G., Bloom, M., Mattress model of lipid–protein interactions in membranes. Biophys J 46 (1984), 141–153.
32. 32 Ramakrishnan, M., Qu, J., Pocanschi, C.L., Kleinschmidt, J.H., Marsh, D., Orientation of β-barrel proteins OmpA and FhuA in lipid membranes. Chain length dependence from infrared dichroism. Biochemistry 44 (2005), 3515–3523.
33. 33 Muhammad, N., Dworeck, T., Fioroni, M., Schwaneberg, U., Engineering of the E. coli outer membrane protein FhuA to overcome the hydrophobic mismatch in thick polymeric membranes. J Nanobiotechnol 9 (2011), 1–9.
34. 34 Stoddart, D., Ayub, M., Höfler, L., Raychaudhuri, P., Klingelhoefer, J.W., Maglia, G., Heron, A., Bayley, H., Functional truncated membrane pores. Proc Natl Acad Sci U S A 111 (2014), 2425–2430.
35. 35 Korkmaz, F., van Pee, K., Yildiz, Ö., IR-spectroscopic characterization of an elongated OmpG mutant. Arch Biochem Biophys 576 (2015), 73–79.
36. 36 Krewinkel, M., Dworeck, T., Fioroni, M., Engineering of an E. coli outer membrane protein FhuA with increased channel diameter. J Nanobiotechnol 9 (2011), 1–8.
37. 37 Reina, S., Magrì, A., Lolicato, M., Guarino, F., Impellizzeri, A., Maier, E., Benz, R., Ceccarelli, M., De Pinto, V., Messina, A., Deletion of β-strands 9 and 10 converts VDAC1 voltage-dependence in an asymmetrical process. Biochim Biophys Acta (BBA) Bioenerg 1827 (2013), 793–805.
38. 38 Koebnik, R., Braun, V., Insertion derivatives containing segments of up to 16 amino acids identify surface- and periplasm-exposed regions of the FhuA outer membrane receptor of Escherichia coli k-12. J Bacteriol 175 (1993), 826–839.
39. 39 Killmann, H., Benz, R., Braun, V., Conversion of the FhuA transport protein into a diffusion channel through the outer membrane of Escherichia coli. EMBO J 12 (1993), 3007–3016.
40. 40 Locher, K.P., Rees, B., Koebnik, R., Mitschler, A., Moulinier, L., Rosenbusch, J.P., Moras, D., Transmembrane signaling across the ligand-gated FhuA receptor: crystal structures of free and ferrichrome-bound states reveal allosteric changes. Cell 95 (1998), 771–778.
41. 41 Braun, M., Killmann, H., Maier, E., Benz, R., Braun, V., Diffusion through channel derivatives of the Escherichia coli FhuA transport protein. Eur J Biochem, 269, 2002.
42. 42 Mohammad, M.M., Howard, K.R., Movileanu, L., Redesign of a plugged β-barrel membrane protein. J Biol Chem 286 (2011), 8000–8013.
43. 43 Wolfe, A.J., Mohammad, M.M., Thakur, A.K., Movileanu, L., Global redesign of a native β-barrel scaffold. Biochim Biophys Acta (BBA) Biomembr 1858 (2016), 19–29.
44. 44 Mapingire, O.S., Henderson, N.S., Duret, G., Thanassi, D.G., Delcour, A.H., Modulating effects of the plug, helix, and N- and C-terminal domains on channel properties of the PapC usher. J Biol Chem 284 (2009), 36324–36333.
45. 45 Jung, Y., Cheley, S., Braha, O., Bayley, H., The internal cavity of the staphylococcal α-hemolysin pore accommodates ∼175 exogenous amino acid residues. Biochemistry 44 (2005), 8919–8929.
46. 46 Urry, D.W., Long, M.M., Sugano, H., Cyclic analog of elastin polyhexapeptide exhibits an inverse temperature transition leading to crystallization. J Biol Chem 253 (1978), 6301–6302.
47. 47 Jung, Y., Bayley, H., Movileanu, L., Temperature-responsive protein pores. J Am Chem Soc 128 (2006), 15332–15340.
48. 48 Saint, N., Lou, K.-L., Widmer, C., Luckey, M., Schirmer, T., Rosenbusch, J.P., Structural and functional characterization of OmpF porin mutants selected for larger pore size. J Biol Chem 271 (1996), 20676–20680.
49. 49 Phale, P.S., Philippsen, A., Widmer, C., Phale, V.P., Rosenbusch, J.P., Schirmer, T., Role of charged residues at the OmpF porin channel constriction probed by mutagenesis and simulation. Biochemistry 40 (2001), 6319–6325.
50. 50 Miedema, H., Meter-Arkema, A., Wierenga, J., Tang, J., Eisenberg, B., Nonner, W., Hektor, H., Gillespie, D., Meijberg, W., Permeation properties of an engineered bacterial OmpF porin containing the EEEE-locus of Ca2+ channels. Biophys J 87 (2004), 3137–3147.
51. 51 Saxena, K., Drosou, V., Maier, E., Benz, R., Ludwig, B., Ion selectivity reversal and induction of voltage-gating by site-directed mutations in the Paracoccus denitrificans porin. Biochemistry 38 (1999), 2206–2212.
52. 52•• Braha, O., Walker, B., Cheley, S., Kasianowicz, J.J., Song, L., Gouaux, J.E., Bayley, H., Designed protein pores as components for biosensors. Chem Biol 4 (1997), 497–505 The authors engineer a divalent metal binding site into α-hemolysin using four histidines on a single beta hairpin. They combine the mutated monomer with six wildtype α-hemolysins in order to create the successful metal binding heptamer. This is the first metal binding site engineered into an outer membrane protein.
53. 53 Ye, Y., Lee, H.-W., Yang, W., Shealy, S.J., Wilkins, A.L., Liu, Z.-R., Torshin, I., Harrison, R., Wohlhueter, R., Yang, J.J., Metal binding affinity and structural properties of an isolated EF-loop in a scaffold protein. Protein Eng 14 (2001), 1001–1013.
54. 54 Johansson, M.U., Alioth, S., Hu, K., Walser, R., Koebnik, R., Pervushin, K., A minimal transmembrane β-barrel platform protein studied by nuclear magnetic resonance. Biochemistry 46 (2007), 1128–1140.
55. 55 Varadarajan, N., Gam, J., Olsen, M.J., Georgiou, G., Iverson, B.L., Engineering of protease variants exhibiting high catalytic activity and exquisite substrate selectivity. Proc Natl Acad Sci U S A 102 (2005), 6855–6860.
56. 56•• Varadarajan, N., Rodriguez, S., Hwang, B.-Y., Georgiou, G., Iverson, B.L., Highly active and selective endopeptidases with programmed substrate specificities. Nat Chem Biol 4 (2008), 290–294 Iverson and colleagues invented a screen for endopeptidase OmpT utilizing a ligand that contains a positive charged fluorophore linked by a peptide to a quencher. If OmpT cleaves the peptide, the fluorophore sticks to the negatively charged surface of E. coli and the cell can be isolated through FACS. In this paper they changed the peptide and heavily mutate the binding site to screen for OmpT variants that would cleave the peptides used. This paper details five endopeptidases which they created with cleavage specificity for an impressive variety of peptides.
57. 57 Varadarajan, N., Georgiou, G., Iverson, B.L., An engineered protease that cleaves specifically after sulfated tyrosine. Angew Chem 120 (2008), 7979–7981.
58. 58 Varadarajan, N., Pogson, M., Georgiou, G., Iverson, B.L., Proteases that can distinguish among different post-translational forms of tyrosine engineered using multicolor flow cytometry. J Am Chem Soc 131 (2009), 18186–18190.
59. 59•• Koebnik, R., In vivo membrane assembly of split variants of the E. coli outer membrane protein OmpA. EMBO J 15 (1996), 3529–3537 Here, Koebnik creates the first novel topology for an outer membrane protein. By splitting OmpA's eight strands into two separate four-stranded constructs, he finds that these constructs bind together to make an eight stranded protein that is heat modifiable and that confers phage sensitivity phenotype. Tantalizingly, he also finds that a six-stranded construct co-expressed with a four-stranded construct functions moderately well.
60. 60 Krauson, A.J., He, J., Wimley, A.W., Hoffmann, A.R., Wimley, W.C., Synthetic molecular evolution of pore-forming peptides by iterative combinatorial library screening. ACS Chem Biol 8 (2013), 823–831.
61. 61 Slusky, J.S.G., Dunbrack, R.L., Charge asymmetry in the proteins of the outer membrane. Bioinformatics 29 (2013), 2122–2128.
62. 62• Alford, R.F., Koehler Leman, J., Weitzner, B.D., Duran, A.M., Tilley, D.C., Elazar, A., Gray, J.J., An integrated framework advancing membrane protein modeling and design. PLoS Comput Biol, 11, 2015, e1004398 This paper describes a membrane focused update of the widely successful protein design software ROSETTA.The update allows for the storing of membrane specific information such as membrane potentials, and preferred movements in the membrane.
63. 63• Lin, M., Gessmann, D., Naveed, H., Liang, J., Outer membrane protein folding and topology from a computational transfer free energy scale. J Am Chem Soc 138 (2016), 2592–2601 This paper describes an update to the membrane potential, TmSIP. This computational potential now includes intrastrand side-chain interactions and an asymmetric membrane. It can be used to calculate ΔΔG values for mutations in OmpLA and can predict the membrane insertion direction.
64. 64 Packer, M.S., Liu, D.R., Methods for the directed evolution of proteins. Nat Rev Genet 16 (2015), 379–394.
65. 65 Scott, D.J., Plückthun, A., Direct molecular evolution of detergent-stable G protein-coupled receptors using polymer encapsulated cells. J Mol Biol 425 (2013), 662–677.
66. 66 McIsaac, R.S., Engqvist, M.K.M., Wannier, T., Rosenthal, A.Z., Herwig, L., Flytzanis, N.C., Imasheva, E.S., Lanyi, J.K., Balashov, S.P., Gradinaru, V., Arnold, F.H., Directed evolution of a far-red fluorescent rhodopsin. Proc Natl Acad Sci U S A 111 (2014), 13034–13039.