Deuterium Labeling Together with Contrast Variation Small-Angle Neutron Scattering Suggests How Skp Captures and Releases Unfolded Outer Membrane Proteins

Methods in Enzymology

Volumn 566, Issue , 2016, Pages 159-210

  Zaccai, Nathan R ^a   Sandlin, Clifford W ^a   Hoopes, James T ^b   Curtis, Joseph E ^c   Fleming, Patrick J ^a   Fleming, Karen G ^a   Krueger, Susan ^c  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b UNIVERSITY OF MARYLAND   (United States)

^c NATIONAL INSTITUTE OF STANDARDS AND TECHNOLOGY   (United States)

Author keywords

Disordered protein; Holdase; Jellyfish like chaperone; Outer membrane protein (OMP) transport; Periplasm; SANS; Skp; Small angle neutron scattering

Indexed keywords

DEUTERIUM; OMPW PROTEIN; OUTER MEMBRANE PROTEIN; OUTER MEMBRANE PROTEIN A; S PHASE KINASE ASSOCIATED PROTEIN; UNCLASSIFIED DRUG; UNFOLDED OUTER MEMBRANE PROTEIN; CONTRAST MEDIUM; SOLUTION AND SOLUBILITY;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL OUTER MEMBRANE; CELL STRUCTURE; CRYSTAL STRUCTURE; DENSITY; GENETIC VARIABILITY; ISOTOPE LABELING; MOLECULAR DYNAMICS; MOLECULAR WEIGHT; NEUTRON SCATTERING; OLIGOMERIZATION; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN PURIFICATION; PROTEIN SECRETION; PROTEIN STRUCTURE; SIMULATION; STOICHIOMETRY; SURFACE PROPERTY; VALIDATION STUDY; X RAY CRYSTALLOGRAPHY; CHEMISTRY; CRYSTALLOGRAPHY; HUMAN; NEUTRON; PERIPLASM; PROCEDURES; SMALL ANGLE SCATTERING; SOLUTION AND SOLUBILITY; STAINING; X RAY DIFFRACTION;

BACTERIAL OUTER MEMBRANE PROTEINS; CONTRAST MEDIA; CRYSTALLOGRAPHY; DEUTERIUM; HUMANS; NEUTRONS; PERIPLASM; S-PHASE KINASE-ASSOCIATED PROTEINS; SCATTERING, SMALL ANGLE; SOLUTIONS; STAINING AND LABELING; X-RAY DIFFRACTION;

EID: 84954392993     PISSN: 00766879     EISSN: 15577988     Source Type: Book Series    
DOI: 10.1016/bs.mie.2015.06.041     Document Type: Chapter

References (81)

1. N.S. Berrow, D. Alderton, S. Sainsbury, J. Nettleship, R. Assenberg, N. Rahman, and et al. A versatile ligation-independent cloning method suitable for high-throughput expression screening applications Nucleic Acids Research 35 2007 e45
2. K.N. Beverly, M.R. Sawaya, E. Schmid, and C.M. Koehler The Tim8-Tim13 complex has multiple substrate binding sites and binds cooperatively to Tim23 Journal of Molecular Biology 382 2008 1144 1156
3. E. Bitto, and D.B. McKay The periplasmic molecular chaperone protein SurA binds a peptide motif that is characteristic of integral outer membrane proteins The Journal of Biological Chemistry 278 2003 49316 49322
4. P.V. Bulieris, S. Behrens, O. Holst, and J.H. Kleinschmidt Folding and insertion of the outer membrane protein OmpA is assisted by the chaperone Skp and by lipopolysaccharide The Journal of Biological Chemistry 278 2003 9092 9099
5. N.K. Burgess, T.P. Dao, A.M. Stanley, and K.G. Fleming Beta-barrel proteins that reside in the Escherichia coli outer membrane in vivo demonstrate varied folding behavior in vitro The Journal of Biological Chemistry 283 2008 26748 26758
6. B.M. Burmann, and S. Hiller Solution NMR studies of membrane-protein-chaperone complexes Chimia 66 2012 759 763
7. B.M. Burmann, D.A. Holdbrook, M. Callon, P.J. Bond, and S. Hiller Revisiting the interaction between the chaperone Skp and lipopolysaccharide Biophysical Journal 108 2015 1516 1526
8. B.M. Burmann, C. Wang, and S. Hiller Conformation and dynamics of the periplasmic membrane-protein-chaperone complexes OmpX-Skp and tOmpA-Skp Nature Structural & Molecular Biology 20 2013 1265 1272
9. M. Callon, B.M. Burmann, and S. Hiller Structural mapping of a chaperone-substrate interaction surface Angewandte Chemie (International Ed. in English) 53 2014 5069 5072
10. R. Chen, and U. Henning A periplasmic protein (Skp) of Escherichia coli selectively binds a class of outer membrane proteins Molecular Microbiology 19 1996 1287 1294
11. J. Chen, W. Im, and C.L. Brooks Application of torsion angle molecular dynamics for efficient sampling of protein conformations Journal of Computational Chemistry 26 2005 1565 1578
12. N.J. Clark, H. Zhang, S. Krueger, H.J. Lee, R.R. Ketchem, B. Kerwin, and et al. Small-angle neutron scattering study of a monoclonal antibody using free-energy constraints The Journal of Physical Chemistry B 117 2013 14029 14038
13. J.E. Curtis, S. Raghunandan, H. Nanda, and S. Krueger SASSIE: A program to study intrinsically disordered biological molecules and macromolecular ensembles using experimental scattering restraints Computer Physics Communications 183 2012 382 389
14. E.J. Danoff, and K.G. Fleming The soluble, periplasmic domain of OmpA folds as an independent unit and displays chaperone activity by reducing the self-association propensity of the unfolded OmpA transmembrane β-barrel Biophysical Chemistry 159 2011 194 204
15. H. De Cock, U. Schäfer, M. Potgeter, R. Demel, M. Müller, and J. Tommassen Affinity of the periplasmic chaperone Skp of Escherichia coli for phospholipids, lipopolysaccharides and non-native outer membrane proteins. Role of Skp in the biogenesis of outer membrane protein European Journal of Biochemistry/FEBS 259 1999 96 103
16. K. Denoncin, J. Schwalm, D. Vertommen, T.J. Silhavy, and J.-F. Collet Dissecting the Escherichia coli periplasmic chaperone network using differential proteomics Proteomics 12 2012 1391 1401
17. D. Engelman, and P.B. Moore Determination of quaternary structure by small-angle neutron scattering Quarterly Reviews of Biophysics 4 1975 219 241
18. K.C. Entzminger, C. Chang, R.O. Myhre, K.C. McCallum, and J.A. Maynard The Skp chaperone helps fold soluble proteins in vitro by inhibiting aggregation Biochemistry 51 2012 4822 4834
19. P.J. Fleming, and G.D. Rose Conformational properties of unfolded proteins J. Buckner, T. Kiefhaber, Protein folding handbook vol. 2 2005 Wiley-VCH Weinheim, Germany 710 736
20. O. Glatter A new method for the evaluation of small-angle scattering data Journal of Applied Crystallography 10 1977 415 421
21. O. Glatter, and O. Kratky Small-angle X-ray scattering 1982 Academic Press New York
22. C.J. Glinka, J.G. Barker, B. Hammouda, S. Krueger, J.J. Moyer, and W.J. Orts The 30 m small-angle neutron scattering instruments at the national institute of standards and technology Journal of Applied Crystallography 31 1998 430 445
23. S. Grizot, and S.K. Buchanan Structure of the OmpA-like domain of RmpM from Neisseria meningitidis Molecular Microbiology 51 2004 1027 1037
24. A. Guinier, and G. Fournet Small-angle scattering of X-rays 1955 John Wiley & Sons, Inc. New York
25. S. Hansen Calculation of small-angle scattering profiles using Monte Carlo simulation Journal of Applied Crystallography 23 1990 344 346
26. N. Harms, G. Koningstein, W. Dontje, M. Muller, B. Oudega, J. Luirink, and et al. The early interaction of the outer membrane protein PhoE with the periplasmic chaperone Skp occurs at the cytoplasmic membrane The Journal of Biological Chemistry 276 2001 18804 18811
27. D.B. Heidorn, and J. Trewhella Comparison of the crystal and solution structures of calmodulin and troponin C Biochemistry 27 1988 909 915
28. W.T. Heller Small-angle neutron scattering and contrast variation: A powerful combination for studying biological structures Acta Crystallographica Section D: Biological Crystallography 66 2010 1213 1217
29. H. Hong, D.R. Patel, L.K. Tamm, and B. van den Berg The outer membrane protein OmpW forms an eight-stranded beta-barrel with a hydrophobic channel The Journal of Biological Chemistry 281 2006 7568 7577
30. K. Ibel, and H.B. Stuhrmann Comparison of neutron and X-ray scattering of dilute myoglobin solutions Journal of Molecular Biology 93 1975 255 265
31. R. Ieva, P. Tian, J.H. Peterson, and H.D. Bernstein Sequential and spatially restricted interactions of assembly factors with an autotransporter beta domain Proceedings of the National Academy of Sciences of the United States of America 108 2011 E383 E391
32. D.A. Jacques, and J. Trewhella Small-angle scattering for structural biology - Expanding the frontier while avoiding the pitfalls Protein Science 19 2010 642 657
33. B. Jacrot The study of biological structures by neutron scattering from solution Reports on Progress in Physics 39 1976 911 953
34. S. Jarchow, C. Lück, A. Görg, and A. Skerra Identification of potential substrate proteins for the periplasmic Escherichia coli chaperone Skp Proteomics 8 2008 4987 4994
35. S.R. Kline Reduction and analysis of SANS and USANS data using IGOR Pro Journal of Applied Crystallography 39 2006 895 900
36. I.P. Korndörfer, M.K. Dommel, and A. Skerra Structure of the periplasmic chaperone Skp suggests functional similarity with cytosolic chaperones despite differing architecture Nature Structural & Molecular Biology 11 2004 1015 1020
37. S. Krueger, I. Gorshkova, J. Brown, J. Hoskins, K.H. McKenney, and F.P. Schwarz Determination of the conformations of cAMP receptor protein and its T127L, S128A mutant with and without cAMP from small angle neutron scattering measurements Journal of Biological Chemistry 273 1998 20001 20006
38. S. Krueger, J.-H. Shin, J.E. Curtis, K.A. Rubinson, and Z. Kelman The solution structure of full-length dodecameric MCM by SANS and molecular modeling: Structure of dodecameric MCM helicase Proteins: Structure, Function, and Bioinformatics 82 2014 2364 2374
39. S. Krueger, J.-H. Shin, S. Raghunandan, J.E. Curtis, and Z. Kelman Atomistic ensemble modeling and small-angle neutron scattering of intrinsically disordered protein complexes: Applied to minichromosome maintenance protein Biophysical Journal 101 2011 2999 3007
40. J. Li, C. Shi, Y. Gao, K. Wu, P. Shi, C. Lai, and et al. Structural studies of Mycobacterium tuberculosis Rv0899 reveal a monomeric membrane-anchoring protein with two separate domains Journal of Molecular Biology 415 2012 382 392
41. V.F. Lundin, P.C. Stirling, J. Gomez-Reino, J.C. Mwenifumbo, J.M. Obst, J.M. Valpuesta, and et al. Molecular clamp mechanism of substrate binding by hydrophobic coiled-coil residues of the archaeal chaperone prefoldin Proceedings of the National Academy of Sciences of the United States of America 101 2004 4367 4372
42. Z.-X. Lyu, Q. Shao, Y.Q. Gao, and X.S. Zhao Direct observation of the uptake of outer membrane proteins by the periplasmic chaperone Skp PLoS One 7 2012 e46068
43. A.D. MacKerell, D. Bashford, Dunbrack Bellott, R.L. Evanseck, J.D. Field, and et al. All-atom empirical potential for molecular modeling and dynamics studies of proteins The Journal of Physical Chemistry B 102 1998 3586 3616
44. J. Martín-Benito, J. Boskovic, P. Gómez-Puertas, J.L. Carrascosa, C.T. Simons, S.A. Lewis, and et al. Structure of eukaryotic prefoldin and of its complexes with unfolded actin and the cytosolic chaperonin CCT The EMBO Journal 21 2002 6377 6386
45. J. Martín-Benito, J. Gómez-Reino, P.C. Stirling, V.F. Lundin, P. Gómez-Puertas, J. Boskovic, and et al. Divergent substrate-binding mechanisms reveal an evolutionary specialization of eukaryotic prefoldin compared to its archaeal counterpart Structure 15 2007 101 110
46. L.M. McMorran, A.I. Bartlett, G.H.M. Huysmans, S.E. Radford, and D.J. Brockwell Dissecting the effects of periplasmic chaperones on the in vitro folding of the outer membrane protein PagP Journal of Molecular Biology 425 2013 3178 3191
47. C.P. Moon, N.R. Zaccai, P.J. Fleming, D. Gessmann, and K.G. Fleming Membrane protein thermodynamic stability may serve as the energy sink for sorting in the periplasm Proceedings of the National Academy of Sciences of the United States of America 110 2013 4285 4290
48. P.B. Moore Small-angle scattering techniques for the study of biological macromolecules and macromolecular aggregates G. Ehrenstein, H. Lecar, Methods of experimental physics vol. 20 1982 Academic Press New York 337 390
49. G.J. Patel, S. Behrens-Kneip, O. Holst, and J.H. Kleinschmidt The periplasmic chaperone Skp facilitates targeting, insertion, and folding of OmpA into lipid membranes with a negative membrane surface potential Biochemistry 48 2009 10235 10245
50. A. Pautsch, and G.E. Schulz Structure of the outer membrane protein A transmembrane domain Nature Structural Biology 5 1998 1013 1017
51. Y. Peng, J.E. Curtis, X. Fang, and S.A. Woodson Structural model of an mRNA in complex with the bacterial chaperone Hfq Proceedings of the National Academy of Sciences of the United States of America 111 2014 17134 17139
52. J.C. Phillips, R. Braun, W. Wang, J. Gumbart, E. Tajkhorshid, E. Villa, and et al. Scalable molecular dynamics with NAMD Journal of Computational Chemistry 26 2005 1781 1802
53. C.D. Putnam, M. Hammel, G.L. Hura, and J.A. Tainer X-ray solution scattering (SAXS) combined with crystallography and computation: Defining accurate macromolecular structures, conformations and assemblies in solution Quarterly Reviews of Biophysics 40 2007 191 285
54. J. Qu, C. Mayer, S. Behrens, O. Holst, and J.H. Kleinschmidt The trimeric periplasmic chaperone Skp of Escherichia coli forms 1:1 complexes with outer membrane proteins via hydrophobic and electrostatic interactions Journal of Molecular Biology 374 2007 91 105
55. R.P. Rambo, and J.A. Tainer Bridging the solution divide: Comprehensive structural analyses of dynamic RNA, DNA, and protein assemblies by small-angle X-ray scattering Current Opinion in Structural Biology 20 2010 128 137
56. Ramelot, T. A., Zhao, L., Hamilton, K., Maglaqui, M., Xiao, R., Liu, J., et al. (unpublished). Solution NMR structure of the folded C-terminal fragment of YiaD from Escherichia coli. Northeast structural genomics consortium target ER553.
57. REDUX. (n.d.). http://pages.jh.edu/pfleming/sw/redux/; retrieved 20 April 2015.
58. V.A. Rhodius, W.C. Suh, G. Nonaka, J. West, and C.A. Gross Conserved and variable functions of the sigmaE stress response in related genomes PLoS Biology 4 2006 e2
59. K.L. Sarachan, J.E. Curtis, and S. Krueger Small-angle scattering contrast calculator for protein and nucleic acid complexes in solution Journal of Applied Crystallography 46 2013 1889 1893
60. SASSIE-web:Beta. (n.d.). https://sassie-web.chem.utk.edu/sassie2/; retrieved 19 June 2015.
61. U. Schäfer, K. Beck, and M. Müller Skp, a molecular chaperone of gram-negative bacteria, is required for the formation of soluble periplasmic intermediates of outer membrane proteins The Journal of Biological Chemistry 274 1999 24567 24574
62. M. Schlapschy, M.K. Dommel, K. Hadian, M. Fogarasi, I.P. Korndörfer, and A. Skerra The periplasmic E. coli chaperone Skp is a trimer in solution: Biophysical and preliminary crystallographic characterization Biological Chemistry 385 2004 137 143
63. J. Schwalm, T.F. Mahoney, G.R. Soltes, and T.J. Silhavy Role for Skp in LptD assembly in Escherichia coli Journal of Bacteriology 195 2013 3734 3742
64. T. Schwede, J. Kopp, N. Guex, and M.C. Peitsch SWISS-MODEL: An automated protein homology-modeling server Nucleic Acids Research 31 2003 3381 3385
65. A.V. Semenyuk, and D.I. Svergun GNOM - A program package for small-angle scattering data processing Journal of Applied Crystallography 24 1991 537 540
66. R. Siegert, M.R. Leroux, C. Scheufler, F.U. Hartl, and I. Moarefi Structure of the molecular chaperone prefoldin: Unique interaction of multiple coiled coil tentacles with unfolded proteins Cell 103 2000 621 632
67. 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 & Development 21 2007 2473 2484
68. P.C. Stirling, S.F. Bakhoum, A.B. Feigl, and M.R. Leroux Convergent evolution of clamp-like binding sites in diverse chaperones Nature Structural & Molecular Biology 13 2006 865 870
69. The PyMOL Molecular Graphics System (version 1.7.4). (n.d.). Schrödinger, LLC.
70. M.A.S. Vergnolle, C. Baud, A.P. Golovanov, F. Alcock, P. Luciano, L.-Y. Lian, and et al. Distinct domains of small Tims involved in subunit interaction and substrate recognition Journal of Molecular Biology 351 2005 839 849
71. J. Vogt, and G.E. Schulz The structure of the outer membrane protein OmpX from Escherichia coli reveals possible mechanisms of virulence Structure (London, England: 1993) 7 1999 1301 1309
72. T.A. Walton, C.M. Sandoval, C.A. Fowler, A. Pardi, and M.C. Sousa The cavity-chaperone Skp protects its substrate from aggregation but allows independent folding of substrate domains Proceedings of the National Academy of Sciences of the United States of America 106 2009 1772 1777
73. T.A. Walton, and M.C. Sousa Crystal structure of Skp, a prefoldin-like chaperone that protects soluble and membrane proteins from aggregation Molecular Cell 15 2004 367 374
74. C.T. Webb, M.A. Gorman, M. Lazarou, M.T. Ryan, and J.M. Gulbis Crystal structure of the mitochondrial chaperone TIM9.10 reveals a six-bladed alpha-propeller Molecular Cell 21 2006 123 133
75. C.T. Webb, E. Heinz, and T. Lithgow Evolution of the β-barrel assembly machinery Trends in Microbiology 20 2012 612 620
76. A.E. Whitten, S. Cai, and J. Trewhella MULCh: Modules for the analysis of small-angle neutron contrast variation data from biomolecular assemblies Journal of Applied Crystallography 41 2008 222 226
77. A.E. Whitten, D.A. Jacques, B. Hammouda, T. Hanley, G.F. King, J.M. Guss, and et al. The structure of the KinA-Sda complex suggests an allosteric mechanism of histidine kinase inhibition Journal of Molecular Biology 368 2007 407 420
78. A.E. Whitten, and J. Trewhella Small-angle scattering and neutron contrast variation for studying bio-molecular complexes R.S. Foote, J.W. Lee, Micro and nano technologies in bioanalysis vol. 544 2009 Humana Press Totowa, NJ 307 323
79. S. Wu, X. Ge, Z. Lv, Z. Zhi, Z. Chang, and X.S. Zhao Interaction between bacterial outer membrane proteins and periplasmic quality control factors: A kinetic partitioning mechanism Biochemical Journal 438 2011 505 511
80. X.-B. Wu, L.-H. Tian, H.-J. Zou, C.-Y. Wang, Z.-Q. Yu, C.-H. Tang, and et al. Outer membrane protein OmpW of Escherichia coli is required for resistance to phagocytosis Research in Microbiology 164 2013 848 855
81. G. Zaccai Straight lines of neutron scattering in biology: A review of basic controls in SANS and EINS European Biophysics Journal 41 2012 781 787