Advertisement

Role of the BAM Complex in Outer Membrane Assembly

  • Fernando Navarro-Garcia
Reference work entry
Part of the Handbook of Hydrocarbon and Lipid Microbiology book series (HHLM)

Abstract

Gram-negative bacteria have a highly evolved cell wall with two membranes constituting a cell envelope consisting of an inner membrane (IM), a periplasmic space, and an outer membrane (OM). Proteins in the bacterial IM contain one or more hydrophobic α-helical transmembrane-spanning domains (TMDs). These co-translationally formed TMDs are accommodated into the IM lipid bilayer through a lateral gate in the Sec complex. While OM proteins (OMPs) reach their destination posttranslationally and contain a unique TMD known as a β-barrel. This amphipathic β-barrel closed cylindrical structure contains 8–26 TMDs that are arranged in a linear antiparallel β-sheet, with the first and last strands interacting at a junction to form this barrel-like shape. OMPs must be transported across the IM, periplasm, and peptidoglycan before they are inserted into the OM to achieve their functional form. The nascent OMPs pass the IM in an unfolded state (uOMPs) with an amino-terminal leader sequence that directs them to the Sec export machinery, which transports the uOMPs into the periplasm, where the lack of ATP is another of the various obstacles to overcome. uOMPs are transported across the periplasm, and successive folding and assembly are key for biogenesis, where chaperones and the essential β-barrel assembly machinery (BAM) complex facilitate these processes. In this chapter, I will describe the role of the BAM complex in outer membrane assembly, including the uOMP protection by periplasmic chaperones, and the structural and functional analyses that illustrate how the BAM complex inserts its substrates into the outer membrane.

Notes

Acknowledgment

This work was supported by a Consejo Nacional de Ciencia y Tecnología (Conacyt) Grant (221130). I thank Paul Ugalde-Silva for the artistic work in Fig. 1 and Lucia Chavez-Dueñas for compiling the references with EndNote software.

References

  1. Albrecht R, Schutz M, Oberhettinger P, Faulstich M, Bermejo I, Rudel T, Diederichs K, Zeth K (2014) Structure of BamA, an essential factor in outer membrane protein biogenesis. Acta Crystallogr D Biol Crystallogr 70(Pt 6):1779–1789.  https://doi.org/10.1107/S1399004714007482CrossRefPubMedGoogle Scholar
  2. Bakelar J, Buchanan SK, Noinaj N (2016) The structure of the beta-barrel assembly machinery complex. Science 351(6269):180–186.  https://doi.org/10.1126/science.aad3460CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bergal HT, Hopkins AH, Metzner SI, Sousa MC (2016) The structure of a BamA-BamD fusion illuminates the architecture of the beta-barrel assembly machine core. Structure 24(2):243–251.  https://doi.org/10.1016/j.str.2015.10.030CrossRefPubMedGoogle Scholar
  4. Beveridge TJ (1999) Structures of gram-negative cell walls and their derived membrane vesicles. J Bacteriol 181(16):4725–4733PubMedPubMedCentralGoogle Scholar
  5. Bitto E, McKay DB (2003) The periplasmic molecular chaperone protein SurA binds a peptide motif that is characteristic of integral outer membrane proteins. J Biol Chem 278(49): 49316–49322.  https://doi.org/10.1074/jbc.M308853200CrossRefPubMedGoogle Scholar
  6. Bos MP, Robert V, Tommassen J (2007) Biogenesis of the gram-negative bacterial outer membrane. Annu Rev Microbiol 61:191–214.  https://doi.org/10.1146/annurev.micro.61.080706.093245CrossRefPubMedGoogle Scholar
  7. Botos I, Noinaj N, Buchanan SK (2017) Insertion of proteins and lipopolysaccharide into the bacterial outer membrane. Philos Trans R Soc Lond Ser B Biol Sci 372(1726).  https://doi.org/10.1098/rstb.2016.0224CrossRefGoogle Scholar
  8. Charlson ES, Werner JN, Misra R (2006) Differential effects of yfgL mutation on Escherichia coli outer membrane proteins and lipopolysaccharide. J Bacteriol 188(20):7186–7194.  https://doi.org/10.1128/JB.00571-06CrossRefPubMedPubMedCentralGoogle Scholar
  9. Costello SM, Plummer AM, Fleming PJ, Fleming KG (2016) Dynamic periplasmic chaperone reservoir facilitates biogenesis of outer membrane proteins. Proc Natl Acad Sci USA 113(33):E4794–E4800.  https://doi.org/10.1073/pnas.1601002113CrossRefPubMedGoogle Scholar
  10. D’Andrea LD, Regan L (2003) TPR proteins: the versatile helix. Trends Biochem Sci 28(12): 655–662.  https://doi.org/10.1016/j.tibs.2003.10.007CrossRefPubMedGoogle Scholar
  11. Danoff EJ, Fleming KG (2015) Membrane defects accelerate outer membrane beta-barrel protein folding. Biochemistry 54(2):97–99.  https://doi.org/10.1021/bi501443pCrossRefPubMedGoogle Scholar
  12. De Geyter J, Tsirigotaki A, Orfanoudaki G, Zorzini V, Economou A, Karamanou S (2016) Protein folding in the cell envelope of Escherichia coli. Nat Microbiol 1(8):16107.  https://doi.org/10.1038/nmicrobiol.2016.107CrossRefPubMedGoogle Scholar
  13. Dong C, Hou HF, Yang X, Shen YQ, Dong YH (2012) Structure of Escherichia coli BamD and its functional implications in outer membrane protein assembly. Acta Crystallogr D Biol Crystallogr 68(Pt 2):95–101.  https://doi.org/10.1107/S0907444911051031CrossRefPubMedGoogle Scholar
  14. Driessen AJ, Nouwen N (2008) Protein translocation across the bacterial cytoplasmic membrane. Annu Rev Biochem 77:643–667.  https://doi.org/10.1146/annurev.biochem.77.061606.160747CrossRefPubMedGoogle Scholar
  15. Gatzeva-Topalova PZ, Walton TA, Sousa MC (2008) Crystal structure of YaeT: conformational flexibility and substrate recognition. Structure 16(12):1873–1881.  https://doi.org/10.1016/j.str.2008.09.014CrossRefPubMedPubMedCentralGoogle Scholar
  16. Gatzeva-Topalova PZ, Warner LR, Pardi A, Sousa MC (2010) Structure and flexibility of the complete periplasmic domain of BamA: the protein insertion machine of the outer membrane. Structure 18(11):1492–1501.  https://doi.org/10.1016/j.str.2010.08.012CrossRefPubMedPubMedCentralGoogle Scholar
  17. Ge X, Wang R, Ma J, Liu Y, Ezemaduka AN, Chen PR, Fu X, Chang Z (2014) DegP primarily functions as a protease for the biogenesis of beta-barrel outer membrane proteins in the Gram-negative bacterium Escherichia coli. FEBS J 281(4):1226–1240.  https://doi.org/10.1111/febs.12701CrossRefPubMedGoogle Scholar
  18. Gessmann D, Chung YH, Danoff EJ, Plummer AM, Sandlin CW, Zaccai NR, Fleming KG (2014) Outer membrane beta-barrel protein folding is physically controlled by periplasmic lipid head groups and BamA. Proc Natl Acad Sci USA 111(16):5878–5883.  https://doi.org/10.1073/pnas.1322473111CrossRefPubMedGoogle Scholar
  19. Grabowicz M, Koren D, Silhavy TJ (2016) The CpxQ sRNA negatively regulates Skp to prevent mistargeting of beta-barrel outer membrane proteins into the cytoplasmic membrane. MBio 7(2):e00312–e00316.  https://doi.org/10.1128/mBio.00312-16CrossRefPubMedPubMedCentralGoogle Scholar
  20. Gu Y, Li H, Dong H, Zeng Y, Zhang Z, Paterson NG, Stansfeld PJ, Wang Z, Zhang Y, Wang W, Dong C (2016) Structural basis of outer membrane protein insertion by the BAM complex. Nature 531(7592):64–69.  https://doi.org/10.1038/nature17199CrossRefPubMedGoogle Scholar
  21. Hagan CL, Kim S, Kahne D (2010) Reconstitution of outer membrane protein assembly from purified components. Science 328(5980):890–892.  https://doi.org/10.1126/science.1188919CrossRefPubMedPubMedCentralGoogle Scholar
  22. Hagan CL, Silhavy TJ, Kahne D (2011) Beta-barrel membrane protein assembly by the Bam complex. Annu Rev Biochem 80:189–210.  https://doi.org/10.1146/annurev-biochem-061408-144611CrossRefPubMedGoogle Scholar
  23. Hagan CL, Westwood DB, Kahne D (2013) Bam lipoproteins assemble BamA in vitro. Biochemistry 52(35):6108–6113.  https://doi.org/10.1021/bi400865zCrossRefPubMedGoogle Scholar
  24. Hagan CL, Wzorek JS, Kahne D (2015) Inhibition of the beta-barrel assembly machine by a peptide that binds BamD. Proc Natl Acad Sci USA 112(7):2011–2016.  https://doi.org/10.1073/pnas.1415955112CrossRefPubMedGoogle Scholar
  25. Harms N, Koningstein G, Dontje W, Muller M, Oudega B, Luirink J, de Cock H (2001) The early interaction of the outer membrane protein phoe with the periplasmic chaperone Skp occurs at the cytoplasmic membrane. J Biol Chem 276(22):18804–18811.  https://doi.org/10.1074/jbc.M011194200.M011194200CrossRefPubMedGoogle Scholar
  26. Heuck A, Schleiffer A, Clausen T (2011) Augmenting beta-augmentation: structural basis of how BamB binds BamA and may support folding of outer membrane proteins. J Mol Biol 406(5): 659–666.  https://doi.org/10.1016/j.jmb.2011.01.002CrossRefPubMedGoogle Scholar
  27. Hu K, Galius V, Pervushin K (2006) Structural plasticity of peptidyl-prolyl isomerase sFkpA is a key to its chaperone function as revealed by solution NMR. Biochemistry 45(39):11983–11991.  https://doi.org/10.1021/bi0607913CrossRefPubMedGoogle Scholar
  28. Jansen KB, Baker SL, Sousa MC (2015) Crystal structure of BamB bound to a periplasmic domain fragment of BamA, the central component of the beta-barrel assembly machine. J Biol Chem 290(4):2126–2136.  https://doi.org/10.1074/jbc.M114.584524CrossRefPubMedGoogle Scholar
  29. Kim S, Malinverni JC, Sliz P, Silhavy TJ, Harrison SC, Kahne D (2007) Structure and function of an essential component of the outer membrane protein assembly machine. Science 317(5840): 961–964.  https://doi.org/10.1126/science.1143993CrossRefPubMedGoogle Scholar
  30. Kim KH, Aulakh S, Tan W, Paetzel M (2011) Crystallographic analysis of the C-terminal domain of the Escherichia coli lipoprotein BamC. Acta Crystallogr Sect F Struct Biol Cryst Commun 67(Pt 11):1350–1358.  https://doi.org/10.1107/S174430911103363XCrossRefPubMedPubMedCentralGoogle Scholar
  31. Kim KH, Aulakh S, Paetzel M (2012) The bacterial outer membrane beta-barrel assembly machinery. Protein Sci Publ Protein Soc 21(6):751–768.  https://doi.org/10.1002/pro.2069CrossRefGoogle Scholar
  32. Knowles TJ, McClelland DM, Rajesh S, Henderson IR, Overduin M (2009) Secondary structure and (1)H, (13)C and (15)N backbone resonance assignments of BamC, a component of the outer membrane protein assembly machinery in Escherichia coli. Biomol NMR Assign 3(2):203–206CrossRefGoogle Scholar
  33. Knowles TJ, Browning DF, Jeeves M, Maderbocus R, Rajesh S, Sridhar P, Manoli E, Emery D, Sommer U, Spencer A, Leyton DL, Squire D, Chaudhuri RR, Viant MR, Cunningham AF, Henderson IR, Overduin M (2011) Structure and function of BamE within the outer membrane and the beta-barrel assembly machine. EMBO Rep 12(2):123–128.  https://doi.org/10.1038/embor.2010.202CrossRefPubMedPubMedCentralGoogle Scholar
  34. Konovalova A, Kahne DE, Silhavy TJ (2017) Outer membrane biogenesis. Annu Rev Microbiol 71:539–556.  https://doi.org/10.1146/annurev-micro-090816-093754CrossRefPubMedPubMedCentralGoogle Scholar
  35. Krojer T, Sawa J, Schafer E, Saibil HR, Ehrmann M, Clausen T (2008) Structural basis for the regulated protease and chaperone function of DegP. Nature 453(7197):885–890.  https://doi.org/10.1038/nature07004CrossRefPubMedGoogle Scholar
  36. Lee J, Xue M, Wzorek JS, Wu T, Grabowicz M, Gronenberg LS, Sutterlin HA, Davis RM, Ruiz N, Silhavy TJ, Kahne DE (2016) Characterization of a stalled complex on the beta-barrel assembly machine. Proc Natl Acad Sci USA 113(31):8717–8722.  https://doi.org/10.1073/pnas.1604100113CrossRefPubMedGoogle Scholar
  37. Matias VR, Al-Amoudi A, Dubochet J, Beveridge TJ (2003) Cryo-transmission electron microscopy of frozen-hydrated sections of Escherichia coli and Pseudomonas aeruginosa. J Bacteriol 185(20):6112–6118CrossRefGoogle Scholar
  38. McMorran LM, Bartlett AI, Huysmans GH, Radford SE, Brockwell DJ (2013) Dissecting the effects of periplasmic chaperones on the in vitro folding of the outer membrane protein PagP. J Mol Biol 425(17):3178–3191.  https://doi.org/10.1016/j.jmb.2013.06.017CrossRefPubMedPubMedCentralGoogle Scholar
  39. Moon CP, Zaccai NR, Fleming PJ, Gessmann D, Fleming KG (2013) Membrane protein thermodynamic stability may serve as the energy sink for sorting in the periplasm. Proc Natl Acad Sci USA 110(11):4285–4290.  https://doi.org/10.1073/pnas.1212527110CrossRefPubMedGoogle Scholar
  40. Murakami Y, Imai M, Nakamura H, Yoshimura F (2002) Separation of the outer membrane and identification of major outer membrane proteins from Porphyromonas gingivalis. Eur J Oral Sci 110(2):157–162CrossRefGoogle Scholar
  41. Ni D, Wang Y, Yang X, Zhou H, Hou X, Cao B, Lu Z, Zhao X, Yang K, Huang Y (2014) Structural and functional analysis of the beta-barrel domain of BamA from Escherichia coli. FASEB J 28(6):2677–2685.  https://doi.org/10.1096/fj.13-248450CrossRefPubMedGoogle Scholar
  42. Nikaido H (2003) Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev MMBR 67(4):593–656CrossRefGoogle Scholar
  43. Noinaj N, Fairman JW, Buchanan SK (2011) The crystal structure of BamB suggests interactions with BamA and its role within the BAM complex. J Mol Biol 407(2):248–260.  https://doi.org/10.1016/j.jmb.2011.01.042CrossRefPubMedPubMedCentralGoogle Scholar
  44. Noinaj N, Kuszak AJ, Gumbart JC, Lukacik P, Chang H, Easley NC, Lithgow T, Buchanan SK (2013) Structural insight into the biogenesis of beta-barrel membrane proteins. Nature 501(7467):385–390.  https://doi.org/10.1038/nature12521CrossRefPubMedPubMedCentralGoogle Scholar
  45. Noinaj N, Kuszak AJ, Balusek C, Gumbart JC, Buchanan SK (2014) Lateral opening and exit pore formation are required for BamA function. Structure 22(7):1055–1062.  https://doi.org/10.1016/j.str.2014.05.008CrossRefPubMedPubMedCentralGoogle Scholar
  46. Noinaj N, Gumbart JC, Buchanan SK (2017) The beta-barrel assembly machinery in motion. Nat Rev Microbiol 15(4):197–204.  https://doi.org/10.1038/nrmicro.2016.191CrossRefPubMedPubMedCentralGoogle Scholar
  47. O’Neil PK, Rollauer SE, Noinaj N, Buchanan SK (2015) Fitting the pieces of the beta-barrel assembly machinery complex. Biochemistry 54(41):6303–6311.  https://doi.org/10.1021/acs.biochem.5b00852CrossRefPubMedPubMedCentralGoogle Scholar
  48. Paschen SA, Waizenegger T, Stan T, Preuss M, Cyrklaff M, Hell K, Rapaport D, Neupert W (2003) Evolutionary conservation of biogenesis of beta-barrel membrane proteins. Nature 426(6968): 862–866.  https://doi.org/10.1038/nature02208CrossRefPubMedGoogle Scholar
  49. Patel GJ, Behrens-Kneip S, Holst O, Kleinschmidt JH (2009) The periplasmic chaperone Skp facilitates targeting, insertion, and folding of OmpA into lipid membranes with a negative membrane surface potential. Biochemistry 48(43):10235–10245.  https://doi.org/10.1021/bi901403cCrossRefPubMedGoogle Scholar
  50. Plummer AM, Fleming KG (2016) From chaperones to the membrane with a BAM! Trends Biochem Sci 41(10):872–882.  https://doi.org/10.1016/j.tibs.2016.06.005CrossRefPubMedPubMedCentralGoogle Scholar
  51. Ricci DP, Hagan CL, Kahne D, Silhavy TJ (2012) Activation of the Escherichia coli beta-barrel assembly machine (Bam) is required for essential components to interact properly with substrate. Proc Natl Acad Sci USA 109(9):3487–3491.  https://doi.org/10.1073/pnas.1201362109CrossRefPubMedGoogle Scholar
  52. Rigel NW, Schwalm J, Ricci DP, Silhavy TJ (2012) BamE modulates the Escherichia coli beta-barrel assembly machine component BamA. J Bacteriol 194(5):1002–1008.  https://doi.org/10.1128/JB.06426-11CrossRefPubMedPubMedCentralGoogle Scholar
  53. Rigel NW, Ricci DP, Silhavy TJ (2013) Conformation-specific labeling of BamA and suppressor analysis suggest a cyclic mechanism for beta-barrel assembly in Escherichia coli. Proc Natl Acad Sci USA 110(13):5151–5156.  https://doi.org/10.1073/pnas.1302662110CrossRefPubMedGoogle Scholar
  54. Rizzitello AE, Harper JR, Silhavy TJ (2001) Genetic evidence for parallel pathways of chaperone activity in the periplasm of Escherichia coli. J Bacteriol 183(23):6794–6800CrossRefGoogle Scholar
  55. Rollauer SE, Sooreshjani MA, Noinaj N, Buchanan SK (2015) Outer membrane protein biogenesis in Gram-negative bacteria. Philos Trans R Soc Lond Ser B Biol Sci 370(1679).  https://doi.org/10.1098/rstb.2015.0023CrossRefGoogle Scholar
  56. Roman-Hernandez G, Peterson JH, Bernstein HD (2014) Reconstitution of bacterial autotransporter assembly using purified components. eLife 3:e04234.  https://doi.org/10.7554/eLife.04234CrossRefPubMedPubMedCentralGoogle Scholar
  57. Sandoval CM, Baker SL, Jansen K, Metzner SI, Sousa MC (2011) Crystal structure of BamD: an essential component of the beta-barrel assembly machinery of gram-negative bacteria. J Mol Biol 409(3):348–357.  https://doi.org/10.1016/j.jmb.2011.03.035CrossRefPubMedPubMedCentralGoogle Scholar
  58. Saul FA, Arie JP, Vulliez-le Normand B, Kahn R, Betton JM, Bentley GA (2004) Structural and functional studies of FkpA from Escherichia coli, a cis/trans peptidyl-prolyl isomerase with chaperone activity. J Mol Biol 335(2):595–608CrossRefGoogle Scholar
  59. Schiffrin B, Calabrese AN, Higgins AJ, Humes JR, Ashcroft AE, Kalli AC, Brockwell DJ, Radford SE (2017) Effects of periplasmic chaperones and membrane thickness on BamA-catalyzed outer-membrane protein folding. J Mol Biol 429(23):3776–3792.  https://doi.org/10.1016/j.jmb.2017.09.008CrossRefPubMedPubMedCentralGoogle Scholar
  60. Sinnige T, Weingarth M, Renault M, Baker L, Tommassen J, Baldus M (2014) Solid-state NMR studies of full-length BamA in lipid bilayers suggest limited overall POTRA mobility. J Mol Biol 426(9):2009–2021.  https://doi.org/10.1016/j.jmb.2014.02.007CrossRefPubMedGoogle Scholar
  61. Sklar JG, Wu T, Kahne D, Silhavy TJ (2007) Defining the roles of the periplasmic chaperones SurA, Skp, and DegP in Escherichia coli. Genes Dev 21(19):2473–2484.  https://doi.org/10.1101/gad.1581007CrossRefPubMedPubMedCentralGoogle Scholar
  62. Soltes GR, Schwalm J, Ricci DP, Silhavy TJ (2016) The activity of Escherichia coli chaperone SurA is regulated by conformational changes involving a parvulin domain. J Bacteriol 198(6): 921–929.  https://doi.org/10.1128/JB.00889-15CrossRefPubMedPubMedCentralGoogle Scholar
  63. Thoma J, Burmann BM, Hiller S, Muller DJ (2015) Impact of holdase chaperones Skp and SurA on the folding of beta-barrel outer-membrane proteins. Nat Struct Mol Biol 22(10):795–802.  https://doi.org/10.1038/nsmb.3087CrossRefPubMedGoogle Scholar
  64. Vogel J, Papenfort K (2006) Small non-coding RNAs and the bacterial outer membrane. Curr Opin Microbiol 9(6):605–611.  https://doi.org/10.1016/j.mib.2006.10.006CrossRefPubMedGoogle Scholar
  65. Voulhoux R, Bos MP, Geurtsen J, Mols M, Tommassen J (2003) Role of a highly conserved bacterial protein in outer membrane protein assembly. Science 299(5604):262–265.  https://doi.org/10.1126/science.1078973CrossRefPubMedGoogle Scholar
  66. Vuong P, Bennion D, Mantei J, Frost D, Misra R (2008) Analysis of YfgL and YaeT interactions through bioinformatics, mutagenesis, and biochemistry. J Bacteriol 190(5):1507–1517.  https://doi.org/10.1128/JB.01477-07CrossRefPubMedGoogle Scholar
  67. Walther DM, Rapaport D, Tommassen J (2009) Biogenesis of beta-barrel membrane proteins in bacteria and eukaryotes: evolutionary conservation and divergence. Cellular Mol Life Sci CMLS 66(17):2789–2804.  https://doi.org/10.1007/s00018-009-0029-zCrossRefPubMedGoogle Scholar
  68. Walton TA, Sousa MC (2004) Crystal structure of Skp, a prefoldin-like chaperone that protects soluble and membrane proteins from aggregation. Mol Cell 15(3):367–374.  https://doi.org/10.1016/j.molcel.2004.07.023CrossRefPubMedGoogle Scholar
  69. Ward R, Zoltner M, Beer L, El Mkami H, Henderson IR, Palmer T, Norman DG (2009) The orientation of a tandem POTRA domain pair, of the beta-barrel assembly protein BamA, determined by PELDOR spectroscopy. Structure 17(9):1187–1194.  https://doi.org/10.1016/j.str.2009.07.011CrossRefPubMedGoogle Scholar
  70. Webb CT, Selkrig J, Perry AJ, Noinaj N, Buchanan SK, Lithgow T (2012) Dynamic association of BAM complex modules includes surface exposure of the lipoprotein BamC. J Mol Biol 422(4):545–555.  https://doi.org/10.1016/j.jmb.2012.05.035CrossRefPubMedPubMedCentralGoogle Scholar
  71. Wu B, Li P, Liu Y, Lou Z, Ding Y, Shu C, Ye S, Bartlam M, Shen B, Rao Z (2004) 3D structure of human FK506-binding protein 52: implications for the assembly of the glucocorticoid receptor/Hsp90/immunophilin heterocomplex. Proc Natl Acad Sci USA 101(22):8348–8353.  https://doi.org/10.1073/pnas.0305969101CrossRefPubMedGoogle Scholar
  72. Wu T, Malinverni J, Ruiz N, Kim S, Silhavy TJ, Kahne D (2005) Identification of a multicomponent complex required for outer membrane biogenesis in Escherichia coli. Cell 121(2):235–245.  https://doi.org/10.1016/j.cell.2005.02.015CrossRefPubMedGoogle Scholar
  73. Wu T, McCandlish AC, Gronenberg LS, Chng SS, Silhavy TJ, Kahne D (2006) Identification of a protein complex that assembles lipopolysaccharide in the outer membrane of Escherichia coli. Proc Natl Acad Sci USA 103(31):11754–11759.  https://doi.org/10.1073/pnas.0604744103CrossRefPubMedGoogle Scholar
  74. Zaccai NR, Sandlin CW, Hoopes JT, Curtis JE, Fleming PJ, Fleming KG, Krueger S (2016) Deuterium labeling together with contrast variation small-angle neutron scattering suggests how Skp captures and releases unfolded outer membrane proteins. Methods Enzymol 566:159–210.  https://doi.org/10.1016/bs.mie.2015.06.041CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Cell BiologyCenter for Research and Advanced Studies (Cinvestav)Mexico CityMexico

Personalised recommendations