A quantitative strategy to detect changes in accessibility of protein regions to chemical modification on heterodimerization

Protein Science

Volumn 18, Issue 7, 2009, Pages 1448-1458

  Dreger, Mathias ^a,c   Bo, Wah Leung ^b   Brownlee, George G ^b   Deng, Tao ^b,d  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c Biochemistry Department   (Germany)

^d NATIONAL INSTITUTE FOR BIOLOGICAL STANDARDS AND CONTROL   (United Kingdom)

Author keywords

Influenza virus polymerase; LC MS MS; NHS biotin; PB1 PA heterodimer; Q POP assay; SILAC

Indexed keywords

BIOTIN; HETERODIMER; LYSINE; MONOMER; N HYDROXYSUCCINIMIDE; N HYDROXYSUCCINIMIDOBIOTIN; RNA POLYMERASE; STABLE ISOTOPE; UNCLASSIFIED DRUG;

ARTICLE; BIOTINYLATION; CELL CULTURE; CELL STRAIN HEK293; CHEMICAL MODIFICATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DIMERIZATION; HUMAN; HUMAN CELL; INFLUENZA; INFLUENZA VIRUS; ISOTOPE LABELING; MASS SPECTROMETRY; MUTAGENESIS; MUTATIONAL ANALYSIS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN INTERACTION; PROTEIN PROTEIN INTERACTION; QUANTITATIVE STRUCTURE ACTIVITY RELATION; STRUCTURAL GENE; SURFACE PROPERTY;

AMINO ACID SEQUENCE; BIOTIN; CHROMATOGRAPHY, LIQUID; DNA MUTATIONAL ANALYSIS; ISOTOPE LABELING; LYSINE; MOLECULAR SEQUENCE DATA; MUTAGENESIS; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN INTERACTION MAPPING; PROTEIN MULTIMERIZATION; PROTEIN SUBUNITS; SEQUENCE ALIGNMENT; SUCCINIMIDES; TANDEM MASS SPECTROMETRY; VIRAL PROTEINS;

ORTHOMYXOVIRIDAE;

EID: 67650086637     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.159     Document Type: Article

References (43)

1. Deng T, Engelhardt OG, Thomas B, Akoulitchev AV, Brownlee GG, Fodor E (2006) Role of ran binding protein 5 in nuclear import and assembly of the influenza virus RNA polymerase complex. J Virol 80:11911-11919.
2. Deng T, Sharps J, Fodor E, Brownlee GG (2005) In vitro assembly of PB2 with a PB1-PA dimer supports a new model of assembly of influenza A virus polymerase subunits into a functional trimeric complex. J Virol 79:8669-8674.
3. Fodor E, Smith M (2004) The PA subunit is required for efficient nuclear accumulation of the PB1 subunit of the influenza A virus RNA polymerase complex. J Virol 78:9144-9153.
4. Gonzalez S, Zurcher T, Ortin J (1996) Identification of two separate domains in the influenza virus PB1 protein involved in the interaction with the PB2 and PA subunits: a model for the viral RNA polymerase structure. Nucleic Acids Res 24:4456-4463.
5. Lee MT, Bishop K, Medcalf L, Elton D, Digard P, Tiley L (2002) Definition of the minimal viral components required for the initiation of unprimed RNA synthesis by influenza virus RNA polymerase. Nucleic Acids Res 30:429-438.
6. Ohtsu Y, Honda Y, Sakata Y, Kato H, Toyoda T (2002) Fine mapping of the subunit binding sites of influenza virus RNA polymerase. Microbiol Immunol 46:167-175.
7. Tsetlin V, Hucho F, Chemische modifikation von proteinen und proteinkomplexen. In: Lottspeich F, Zorbas H, Eds. (1998) Bioanalytik. Heidelberg: Spektrum-Verlag, pp 103-130.
8. Geoghegan KF (2001) Current protocols in protein science, Chapter 5. Wiley Interscience, Wiley-Blackwell, N.J., USA.
9. Ong SE, Foster LJ, Mann M (2003) Mass spectrometric-based approaches in quantitative proteomics. Methods 29:124-130.
10. Abdel-Ghafar AN, Chotpitayasunondh T, Gao Z, Hayden FG, Nguyen DH, de Jong MD, Naghdaliyev A, Peiris JS, Shindo N, Soeroso S, Uyeki TM (2008) Update on avian influenza A (H5N1) virus infection in humans. N Engl J Med 358:261-273.
11. Ghanem A, Mayer D, Chase G, Tegge W, Frank R, Kochs G, Garcia-Sastre A, Schwemmle M (2007) Peptide-mediated interference with influenza A virus polymerase. J Virol 81:7801-7804.
12. He X, Zhou J, Bartlam M, Zhang R, Ma J, Lou Z, Li X, Li J, Joachimiak A, Zeng Z, Ge R, Rao Z, Liu Y (2008) Crystal structure of the polymerase PA(C)-PB1(N) complex from an avian influenza H5N1 virus. Nature 454:1123-1126.
13. Obayashi E, Yoshida H, Kawai F, Shibayama N, Kawaguchi A, Nagata K, Tame JRH, Park S-Y (2008) The structural basis for an essential subunit interaction in influenza virus RNA polymerase. Nature 454:1127-1131.
14. Palese P, Shaw M, Orthomyxoviridae: the viruses and their replication. In: Knipe DM, Howley PM, Eds. (2006) Field virology, 5th ed. Philadelphia: Lippincott, Williams, & Wilkins, pp 1647-1689.
15. Hara K, Schmidt FI, Crow M, Brownlee GG (2006) Amino acid residues in the N-terminal region of the PA subunit of influenza A virus RNA polymerase play a critical role in protein stability, endonuclease activity, cap binding, and virion RNA promoter binding. J Virol 80:7789-7798.
16. Maier HJ, Kashiwagi T, Hara K, Brownlee GG (2008) Differential role of the influenza A virus polymerase PA subunit for vRNA and cRNA promoter binding. Virology 370:194-204.
17. Dias A, Bouvier D, Crepin T, McCarthy AA, Hart DJ, Baudin F, Cusack S, Ruigrok RW (2009) The cap-snatching endonuclease of influenza virus polymerase resides in the PA subunit. Nature 458:914-918.
18. Yuan P, Bartlam M, Lou Z, Chen S, Zhou J, He X, Ly Z, Ge R, Li X, Deng T, Fodor E, Rao Z, Liu Y (2009) Crystal structure of an avian influenza polymerase PA(N) reveals an endonuclease active site. Nature 458:909-913.
19. Torreira E, Schoehn G, Fernandez Y, Jorba N, Ruigrok RW, Cusack S, Ortin J, Llorca O (2007) Three-dimensional model for the isolated recombinant influenza virus polymerase heterotrimer. Nucleic Acids Res 35:3774-3783.
20. Digard P, Blok VC, Inglis SC (1989) Complex formation between influenza virus polymerase proteins expressed in Xenopus oocytes. Virology 171:162-169.
21. Guu TS, Dong L, Wittung-Stafshede P, Tao YJ (2008) Mapping the domain structure of the influenza A virus polymerase acidic protein (PA) and its interaction with the basic protein 1 (PB1) subunit. Virology 379:135-142.
22. Perez DR, Donis RO (2001) Functional analysis of PA binding by influenza a virus PB1: effects on polymerase activity and viral infectivity. J Virol 75:8127-8136.
23. Kuzuhara T, Kise D, Yoshida H, Horita T, Murazaki Y, Nishimura A, Echigo N, Utsunomiya H, Tsuge H (2009) Structural basis of the influenza A virus RNA polymerase PB2 RNA-binding domain containing the pathogenicity-determinant lysine 627 residue. J Biol Chem 284:6855-6860.
24. Tarendeau F, Crepin T, Guilligay D, Ruigrok RW, Cusack S, Hart DJ (2008) Host determinant residue lysine 627 lies on the surface of a discrete, folded domain of influenza virus polymerase PB2 subunit. PLoS Pathog 4:e1000136.
25. Guilligay D, Tarendeau F, Resa-Infante P, Coloma R, Crepin T, Sehr P, Lewis J, Ruigrok RW, Ortin J, Hart DJ, Cusask S (2008) The structural basis for cap binding by influenza virus polymerase subunit PB2. Nat Struct Mol Biol 15:500-506.
26. Hung CW, Schlosser A, Wei J, Lehmann WD (2007) Collision-induced reporter fragmentations for identification of covalently modified peptides. Anal Bioanal Chem 389:1003-1016.
27. Fodor E, Mingay LJ, Crow M, Deng T, Brownlee GG (2003) A single amino acid mutation in the PA subunit of the influenza virus RNA polymerase promotes the generation of defective interfering RNAs. J Virol 77:5017-5020.
28. Kvaratskhelia M, Miller JT, Budihas SR, Pannell LK, Le Grice SF (2002) Identification of specific HIV-1 reverse transcriptase contacts to the viral RNA:tRNA complex by mass spectrometry and a primary amine selective reagent. Proc Natl Acad Sci USA 99:15988-15993.
29. Wales TE, Engen JR (2006) Hydrogen exchange mass spectrometry for the analysis of protein dynamics. Mass Spectrom Rev 25:158-170.
30. Zhao Z, McKee CJ, Kessl JJ, Santos WL, Daigle JE, Engelman A, Verdine G, Kvaratskhelia M (2008) Subunit-specific protein footprinting reveals significant structural rearrangements and a role for N-terminal Lys-14 of HIV-1 integrase during viral DNA binding. J Biol Chem 283:5632-5641.
31. Fanucci GE, Cafiso DS (2006) Recent advances and applications of site-directed spin labeling. Curr Opin Struct Biol 16:644-653.
32. Chase G, Deng T, Fodor E, Leung BW, Mayer D, Schwemmle M, Brownlee G (2008) Hsp90 inhibitors reduce influenza virus replication in cell culture. Virology 377:431-439.
33. Mayer D, Molawi K, Martinez-Sobrido L, Ghanem A, Thomas S, Baginsky S, Grossmann J, Garcia-Sastre A, Schwemmle M (2007) Identification of cellular interaction partners of the influenza virus ribonucleoprotein complex and polymerase complex using proteomic-based approaches. J Proteome Res 6:672-682.
34. Naito T, Momose F, Kawaguchi A, Nagata K (2007) Involvement of Hsp90 in assembly and nuclear import of influenza virus RNA polymerase subunits. J Virol 81:1339-1349.
35. Li ML, Rao P, Krug RM (2001) The active sites of the influenza cap-dependent endonuclease are on different polymerase subunits. EMBO J 20:2078-2086.
36. Poch O, Sauvaget I, Delarue M, Tordo N (1989) Identification of four conserved motifs among the RNA-dependent polymerase encoding elements. EMBO J 8:3867-3874.
37. Kerry PS, Willsher N, Fodor E (2008) A cluster of conserved basic amino acids near the C-terminus of the PB1 subunit of the influenza virus RNA polymerase is involved in the regulation of viral transcription. Virology 373:202-210.
38. Jung TE, Brownlee GG (2006) A new promoter-binding site in the PB1 subunit of the influenza A virus polymerase. J Gen Virol 87:679-688.
39. Fodor E, Devenish L, Engelhardt OG, Palese P, Brownlee GG, Garcia-Sastre A (1999) Rescue of influenza A virus from recombinant DNA. J Virol 73:9679-9682.
40. Puig O, Caspary F, Rigaut G, Rutz B, Bouveret E, Bragado-Nilsson E, Wilm M, Seraphin B (2001) The tandem affinity purification (TAP) method: a general procedure of protein complex purification. Methods 24:218-229.
41. Momose F, Naito T, Yano K, Sugimoto S, Morikawa Y, Nagata K (2002) Identification of Hsp90 as a stimulatory host factor involved in influenza virus RNA synthesis. J Biol Chem 277:45306-45314.
42. Vreede FT, Jung TE, Brownlee GG (2004) Model suggesting that replication of influenza virus is regulated by stabilization of replicative intermediates. J Virol 78:9568-9572.
43. Fodor E, Crow M, Mingay LJ, Deng T, Sharps J, Fechter P, Brownlee GG (2002) A single amino acid mutation in the PA subunit of the influenza virus RNA polymerase inhibits endonucleolytic cleavage of capped RNAs. J Virol 76:8989-9001.