Structure of the Membrane Anchor of Pestivirus Glycoprotein Erns, a Long Tilted Amphipathic Helix

PLoS Pathogens

Volumn 10, Issue 2, 2014, Pages

  Aberle, Daniel ^a   Muhle Goll, Claudia ^b   Bürck, Jochen ^b   Wolf, Moritz ^b   Reißer, Sabine ^b   Luy, Burkhard ^b   Wenzel, Wolfgang ^b   Ulrich, Anne S ^b   Meyers, Gregor ^a  

^a FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

^b KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN; SIGNAL PEPTIDASE;

ARTICLE; CIRCULAR DICHROISM; IMMUNE RESPONSE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOLECULAR DYNAMICS; MONTE CARLO METHOD; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PESTIVIRUS; POLYMERASE CHAIN REACTION; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; SEQUENCE ANALYSIS; SIMULATION;

AMINO ACID SEQUENCE; CIRCULAR DICHROISM; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; PESTIVIRUS; PROTEIN STRUCTURE, SECONDARY; VIRAL ENVELOPE PROTEINS;

EID: 84897735065     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003973     Document Type: Article

References (87)

1. Lindenbach BD, Thiel HJ, Rice CM (2007) Flaviviridae: The Viruses and Their Replication. In: Knipe DM, Howley PM, editors. Fields Virology. Philadelphia, New York: Lippincott- Raven Publishers. pp. 1101-1152.
2. Moennig V, Plagemann PG, (1992) The pestiviruses. Advances in virus research 41: 53-98.
3. Thiel HJ, Plagemann PGW, Moennig V (1996) Pestiviruses. In: Fields BN, Knipe DM, Howley PM, editors. Fields Virology. Philadelphia, New York: Lippincott- Raven Publishers. pp. 1059-1073.
4. Meyers G, Ege A, Fetzer C, von Freyburg M, Elbers K, et al. (2007) Bovine viral diarrhea virus: prevention of persistent fetal infection by a combination of two mutations affecting Erns RNase and Npro protease. Journal of virology 81: 3327-3338.
5. Seago J, Hilton L, Reid E, Doceul V, Jeyatheesan J, et al. (2007) The Npro product of classical swine fever virus and bovine viral diarrhea virus uses a conserved mechanism to target interferon regulatory factor-3. The Journal of general virology 88: 3002-3006.
6. Ruggli N, Summerfield A, Fiebach AR, Guzylack-Piriou L, Bauhofer O, et al. (2009) Classical swine fever virus can remain virulent after specific elimination of the interferon regulatory factor 3-degrading function of Npro. Journal of virology 83: 817-829.
7. La Rocca SA, Herbert RJ, Crooke H, Drew TW, Wileman TE, et al. (2005) Loss of interferon regulatory factor 3 in cells infected with classical swine fever virus involves the N-terminal protease, Npro. Journal of virology 79: 7239-7247.
8. Hilton L, Moganeradj K, Zhang G, Chen YH, Randall RE, et al. (2006) The NPro product of bovine viral diarrhea virus inhibits DNA binding by interferon regulatory factor 3 and targets it for proteasomal degradation. Journal of virology 80: 11723-11732.
9. Chen Z, Rijnbrand R, Jangra RK, Devaraj SG, Qu L, et al. (2007) Ubiquitination and proteasomal degradation of interferon regulatory factor-3 induced by Npro from a cytopathic bovine viral diarrhea virus. Virology 366: 277-292.
10. Bauhofer O, Summerfield A, Sakoda Y, Tratschin JD, Hofmann MA, et al. (2007) Classical swine fever virus Npro interacts with interferon regulatory factor 3 and induces its proteasomal degradation. Journal of virology 81: 3087-3096.
11. Fiebach AR, Guzylack-Piriou L, Python S, Summerfield A, Ruggli N, (2011) Classical swine fever virus N(pro) limits type I interferon induction in plasmacytoid dendritic cells by interacting with interferon regulatory factor 7. Journal of virology 85: 8002-8011.
12. Weiland E, Stark R, Haas B, Rumenapf T, Meyers G, et al. (1990) Pestivirus glycoprotein which induces neutralizing antibodies forms part of a disulfide-linked heterodimer. Journal of virology 64: 3563-3569.
13. Weiland F, Weiland E, Unger G, Saalmuller A, Thiel HJ, (1999) Localization of pestiviral envelope proteins E(rns) and E2 at the cell surface and on isolated particles. The Journal of general virology 80 (Pt 5) (): 1157-1165.
14. Hulst MM, Moormann RJ, (2001) Erns protein of pestiviruses. Methods in enzymology 342: 431-440.
15. Rümenapf T, Unger G, Strauss JH, Thiel HJ, (1993) Processing of the envelope glycoproteins of pestiviruses. Journal of virology 67: 3288-3294.
16. Magkouras I, Matzener P, Rumenapf T, Peterhans E, Schweizer M, (2008) RNase-dependent inhibition of extracellular, but not intracellular, dsRNA-induced interferon synthesis by Erns of pestiviruses. The Journal of general virology 89: 2501-2506.
17. Hulst MM, Himes G, Newbigin E, Moormann RJ, (1994) Glycoprotein E2 of classical swine fever virus: expression in insect cells and identification as a ribonuclease. Virology 200: 558-565.
18. Schneider R, Unger G, Stark R, Schneider-Scherzer E, Thiel HJ, (1993) Identification of a structural glycoprotein of an RNA virus as a ribonuclease. Science 261: 1169-1171.
19. Windisch JM, Schneider R, Stark R, Weiland E, Meyers G, et al. (1996) RNase of classical swine fever virus: biochemical characterization and inhibition by virus-neutralizing monoclonal antibodies. Journal of virology 70: 352-358.
20. Krey T, Bontems F, Vonrhein C, Vaney MC, Bricogne G, et al. (2012) Crystal structure of the pestivirus envelope glycoprotein E(rns) and mechanistic analysis of its ribonuclease activity. Structure 20: 862-873.
21. Meyer C, Von Freyburg M, Elbers K, Meyers G, (2002) Recovery of virulent and RNase-negative attenuated type 2 bovine viral diarrhea viruses from infectious cDNA clones. Journal of virology 76: 8494-8503.
22. Meyers G, Saalmuller A, Buttner M, (1999) Mutations abrogating the RNase activity in glycoprotein E(rns) of the pestivirus classical swine fever virus lead to virus attenuation. Journal of virology 73: 10224-10235.
23. Tews BA, Schurmann EM, Meyers G, (2009) Mutation of cysteine 171 of pestivirus E(rns) RNase prevents homodimer formation and leads to attenuation of classical swine fever virus. Journal of virology 83: 4823-4834.
24. Fetzer C, Tews BA, Meyers G, (2005) The carboxy-terminal sequence of the pestivirus glycoprotein E(rns) represents an unusual type of membrane anchor. Journal of virology 79: 11901-11913.
25. Tews BA, Meyers G, (2007) The pestivirus glycoprotein Erns is anchored in plane in the membrane via an amphipathic helix. The Journal of biological chemistry 282: 32730-32741.
26. Burrack S, Aberle D, Burck J, Ulrich AS, Meyers G, (2012) A new type of intracellular retention signal identified in a pestivirus structural glycoprotein. FASEB journal: official publication of the Federation of American Societies for Experimental Biology 26: 3292-3305.
27. Bintintan I, Meyers G, (2010) A new type of signal peptidase cleavage site identified in an RNA virus polyprotein. The Journal of biological chemistry 285: 8572-8584.
28. Nilsson I, Johnson AE, von Heijne G, (2002) Cleavage of a tail-anchored protein by signal peptidase. FEBS letters 516: 106-108.
29. Nilsson I, Whitley P, von Heijne G, (1994) The COOH-terminal ends of internal signal and signal-anchor sequences are positioned differently in the ER translocase. The Journal of cell biology 126: 1127-1132.
30. Walther TH, Gottselig C, Grage SL, Wolf M, Vargiu AV, et al. (2013) Folding and self-assembly of the TatA translocation pore based on a charge zipper mechanism. Cell 152: 316-326.
31. Wu Y, Huang HW, Olah GA, (1990) Method of oriented circular dichroism. Biophysical journal 57: 797-806.
32. Olah GA, Huang HW, (1988) Circular dichroism of oriented alpha-helices. II. Electric field oriented polypeptides. The Journal of Chemical Physics 89: 6956-6962.
33. Bürck J, Roth S, Wadhwani P, Afonin S, Kanithasen N, et al. (2008) Conformation and membrane orientation of amphiphilic helical peptides by oriented circular dichroism. Biophysical journal 95: 3872-3881.
34. Afonin S, Grage SL, Ieronimo M, Wadhwani P, Ulrich AS, (2008) Temperature-dependent transmembrane insertion of the amphiphilic peptide PGLa in lipid bilayers observed by solid state 19F NMR spectroscopy. Journal of the American Chemical Society 130: 16512-16514.
35. Glaser RW, Sachse C, Durr UH, Wadhwani P, Afonin S, et al. (2005) Concentration-dependent realignment of the antimicrobial peptide PGLa in lipid membranes observed by solid-state 19F-NMR. Biophysical journal 88: 3392-3397.
36. Grage SL, Afonin S, Ulrich AS, (2010) Dynamic transitions of membrane-active peptides. Methods in molecular biology 618: 183-207.
37. Strandberg E, Tiltak D, Ehni S, Wadhwani P, Ulrich AS, (2012) Lipid shape is a key factor for membrane interactions of amphipathic helical peptides. Biochimica et biophysica acta 1818: 1764-1776.
38. Strandberg E, Zerweck J, Wadhwani P, Ulrich AS, (2013) Synergistic insertion of antimicrobial magainin-family peptides in membranes depends on the lipid spontaneous curvature. Biophysical journal 104: L9-11.
39. Hilty C, Wider G, Fernandez C, Wuthrich K, (2004) Membrane protein-lipid interactions in mixed micelles studied by NMR spectroscopy with the use of paramagnetic reagents. Chembiochem: a European journal of chemical biology 5: 467-473.
40. Hwang TL, van Zijl PC, Mori S, (1998) Accurate quantitation of water-amide proton exchange rates using the phase-modulated CLEAN chemical EXchange (CLEANEX-PM) approach with a Fast-HSQC (FHSQC) detection scheme. Journal of biomolecular NMR 11: 221-226.
41. Lindorff-Larsen K, Piana S, Palmo K, Maragakis P, Klepeis JL, et al. (2010) Improved side-chain torsion potentials for the Amber ff99SB protein force field. Proteins 78: 1950-1958.
42. Lindorff-Larsen K, Piana S, Dror RO, Shaw DE, (2011) How fast-folding proteins fold. Science 334: 517-520.
43. Shaw DE, Maragakis P, Lindorff-Larsen K, Piana S, Dror RO, et al. (2010) Atomic-level characterization of the structural dynamics of proteins. Science 330: 341-346.
44. SJS CBM WWi, (2013) SLIM: An Improved Generalized Born Implicit Membrane Model. Journal of Chemical Theory and Computation.
45. Meyers G, Rümenapf T, Ziebuhr J (2011) Viral RNase Involvement in Strategies of Infection. In: Nicholson AW, editor. Ribonucleases: Springer Berlin Heidelberg. pp. 135-165.
46. Lazar C, Zitzmann N, Dwek RA, Branza-Nichita N, (2003) The pestivirus E(rns) glycoprotein interacts with E2 in both infected cells and mature virions. Virology 314: 696-705.
47. Cui H, Lyman E, Voth GA, (2011) Mechanism of membrane curvature sensing by amphipathic helix containing proteins. Biophysical journal 100: 1271-1279.
48. Bhatia VK, Madsen KL, Bolinger PY, Kunding A, Hedegard P, et al. (2009) Amphipathic motifs in BAR domains are essential for membrane curvature sensing. The EMBO journal 28: 3303-3314.
49. Prinz WA, Hinshaw JE, (2009) Membrane-bending proteins. Critical reviews in biochemistry and molecular biology 44: 278-291.
50. Pednekar D, Wang Y, Fedotova TV, Wojcikiewicz RJ, (2011) Clustered hydrophobic amino acids in amphipathic helices mediate erlin1/2 complex assembly. Biochemical and biophysical research communications 415: 135-140.
51. Stachowiak JC, Schmid EM, Ryan CJ, Ann HS, Sasaki DY, et al. (2012) Membrane bending by protein-protein crowding. Nature cell biology 14: 944-949.
52. Raghuraman H, Chattopadhyay A, (2007) Melittin: a membrane-active peptide with diverse functions. Bioscience reports 27: 189-223.
53. Berneche S, Nina M, Roux B, (1998) Molecular dynamics simulation of melittin in a dimyristoylphosphatidylcholine bilayer membrane. Biophysical journal 75: 1603-1618.
54. Liu L, Westler WM, den Boon JA, Wang X, Diaz A, et al. (2009) An amphipathic alpha-helix controls multiple roles of brome mosaic virus protein 1a in RNA replication complex assembly and function. PLoS pathogens 5: e1000351.
55. Gouttenoire J, Montserret R, Kennel A, Penin F, Moradpour D, (2009) An amphipathic alpha-helix at the C terminus of hepatitis C virus nonstructural protein 4B mediates membrane association. Journal of virology 83: 11378-11384.
56. Penin F, Brass V, Appel N, Ramboarina S, Montserret R, et al. (2004) Structure and function of the membrane anchor domain of hepatitis C virus nonstructural protein 5A. The Journal of biological chemistry 279: 40835-40843.
57. Moradpour D, Brass V, Penin F, (2005) Function follows form: the structure of the N-terminal domain of HCV NS5A. Hepatology 42: 732-735.
58. Gouttenoire J, Roingeard P, Penin F, Moradpour D, (2010) Amphipathic alpha-helix AH2 is a major determinant for the oligomerization of hepatitis C virus nonstructural protein 4B. Journal of virology 84: 12529-12537.
59. G O, (2010) Protein NMR using paramagnetic ions. Annu Rev Biophys 39: 387-405.
60. Thiel HJ, Stark R, Weiland E, Rumenapf T, Meyers G, (1991) Hog cholera virus: molecular composition of virions from a pestivirus. Journal of virology 65: 4705-4712.
61. van Gennip HG, Hesselink AT, Moormann RJ, Hulst MM, (2005) Dimerization of glycoprotein E(rns) of classical swine fever virus is not essential for viral replication and infection. Archives of virology 150: 2271-2286.
62. Langedijk JP, van Veelen PA, Schaaper WM, de Ru AH, Meloen RH, et al. (2002) A structural model of pestivirus E(rns) based on disulfide bond connectivity and homology modeling reveals an extremely rare vicinal disulfide. Journal of virology 76: 10383-10392.
63. Bogomolovas J, Simon B, Sattler M, Stier G, (2009) Screening of fusion partners for high yield expression and purification of bioactive viscotoxins. Protein expression and purification 64: 16-23.
64. Corpet F, (1988) Multiple sequence alignment with hierarchical clustering. Nucleic acids research 16: 10881-10890.
65. Green MR, Sambrook J (2012) Molecular Cloning: A Laboratory Manual (Fourth Edition): Cold Spring Harbor Laboratory Press.
66. Sreerama N, Venyaminov SY, Woody RW, (2000) Estimation of protein secondary structure from circular dichroism spectra: inclusion of denatured proteins with native proteins in the analysis. Analytical biochemistry 287: 243-251.
67. Johnson WC, (1999) Analyzing protein circular dichroism spectra for accurate secondary structures. Proteins 35: 307-312.
68. van Stokkum IH, Spoelder HJ, Bloemendal M, van Grondelle R, Groen FC, (1990) Estimation of protein secondary structure and error analysis from circular dichroism spectra. Analytical biochemistry 191: 110-118.
69. Provencher SW, Glockner J, (1981) Estimation of globular protein secondary structure from circular dichroism. Biochemistry 20: 33-37.
70. Sreerama N, Woody RW, (1993) A self-consistent method for the analysis of protein secondary structure from circular dichroism. Analytical biochemistry 209: 32-44.
71. Sreerama N, Venyaminov SY, Woody RW, (1999) Estimation of the number of alpha-helical and beta-strand segments in proteins using circular dichroism spectroscopy. Protein science: a publication of the Protein Society 8: 370-380.
72. Whitmore L, Wallace BA, (2004) DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic acids research 32: W668-673.
73. Lobley A, Whitmore L, Wallace BA, (2002) DICHROWEB: an interactive website for the analysis of protein secondary structure from circular dichroism spectra. Bioinformatics 18: 211-212.
74. Windisch D, Hoffmann S, Afonin S, Vollmer S, Benamira S, et al. (2010) Structural role of the conserved cysteines in the dimerization of the viral transmembrane oncoprotein E5. Biophysical journal 99: 1764-1772.
75. Blomberg N, Sattler M, Nilges M, (1999) 1H, 15N, and 13C resonance assignment of the PH domain from C. elegans UNC-89. Journal of biomolecular NMR 15: 269-270.
76. Farrow NA, Muhandiram R, Singer AU, Pascal SM, Kay CM, et al. (1994) Backbone dynamics of a free and phosphopeptide-complexed Src homology 2 domain studied by 15N NMR relaxation. Biochemistry 33: 5984-6003.
77. Kay LE, Torchia DA, Bax A, (1989) Backbone dynamics of proteins as studied by 15N inverse detected heteronuclear NMR spectroscopy: application to staphylococcal nuclease. Biochemistry 28: 8972-8979.
78. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, et al. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. Journal of biomolecular NMR 6: 277-293.
79. Johnson BA, (2004) Using NMRView to visualize and analyze the NMR spectra of macromolecules. Methods Mol Biol 278: 313-352.
80. Strunk T, Wolf M, Brieg M, Klenin K, Biewer A, et al. (2012) SIMONA 1.0: an efficient and versatile framework for stochastic simulations of molecular and nanoscale systems. Journal of computational chemistry 33: 2602-2613.
81. Kabsch W, Sander C, (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22: 2577-2637.
82. Berendsen HvdS, D; van Drunen R, (1995) GROMACS: A message-passing parallel molecular dynamics implementation. Computer Physics Communications 91: 43-56.
83. Case DA, Darden TA, Cheatham, III TE, Simmerling CL, Wang J, et al. (2012) AMBER 12. University of California, San Francisco.
84. Nosé S, (1984) A molecular dynamics method for simulations in the canonical ensemble. Molecular Physics 52: 255-268.
85. Parrinello M, Rahman A, (1981) Polymorphic transitions in single crystals: A new molecular dynamics method. Journal of Applied Physics 52: 7182-7190.
86. Hess B, Bekker H, Berendsen HJC, Fraaije JGEM, (1997) LINCS: A linear constraint solver for molecular simulations. Journal of computational chemistry 18: 1463-1472.
87. de Jongh H H, Goormaghtigh E, Killian J A, (1994) Analysis of circular dichroism spectra of oriented protein-lipid complexes: toward a general application. Biochemistry 33 (48) (): 14521-14528.