Order and disorder control the functional rearrangement of influenza hemagglutinin

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 33, 2014, Pages 12049-12054

  Lin, Xingcheng ^a   Eddy, Nathanial R ^a   Noel, Jeffrey K ^a   Whitford, Paul C ^c   Wang, Qinghua ^d   Ma, Jianpeng ^a,b,d   Onuchic, José N ^a  

^a RICE UNIVERSITY   (United States)

^b Rice University   (United States)

^c NORTHEASTERN UNIVERSITY   (United States)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Protein folding; Structure based model

Indexed keywords

INFLUENZA VIRUS HEMAGGLUTININ;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; ENERGY; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; X RAY CRYSTALLOGRAPHY;

PROTEIN FOLDING; STRUCTURE-BASED MODEL;

HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; MOLECULAR DYNAMICS SIMULATION;

EID: 84906328200     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1412849111     Document Type: Article

References (40)

1. Skehel JJ, Wiley DC (2000) Receptor binding and membrane fusion in virus entry: The influenza hemagglutinin. Annu Rev Biochem 69:531-569.
2. Skehel JJ, Wiley DC (1998) Coiled coils in both intracellular vesicle and viral membrane fusion. Cell 95(7):871-874. (Pubitemid 29019038)
3. Hughson FM (1997) Enveloped viruses: A common mode of membrane fusion? Curr Biol 7(9):R565-R569.
4. Wilson IA, Skehel JJ, Wiley DC (1981) Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution. Nature 289(5796):366-373.
5. Carr CM, Chaudhry C, Kim PS (1997) Influenza hemagglutinin is spring-loaded by a metastable native conformation. Proc Natl Acad Sci USA 94(26):14306-14313. (Pubitemid 28041369)
6. Bullough PA, Hughson FM, Skehel JJ, Wiley DC (1994) Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 371(6492):37-43. (Pubitemid 24277462)
7. Bizebard T, et al. (1995) Structure of influenza virus haemagglutinin complexed with a neutralizing antibody. Nature 376(6535):92-94.
8. Park HE, Gruenke JA, White JM (2003) Leash in the groove mechanism of membrane fusion. Nat Struct Biol 10(12):1048-1053. (Pubitemid 37500497)
9. Melikyan GB, Niles WD, Cohen FS (1995) The fusion kinetics of influenza hemagglutinin expressing cells to planar bilayer membranes is affected by HA density and host cell surface. J Gen Physiol 106(5):783-802.
10. Bentz J (2000) Minimal aggregate size and minimal fusion unit for the first fusion pore of influenza hemagglutinin-mediated membrane fusion. Biophys J 78(1):227-245.
11. Bentz J (2000) Membrane fusion mediated by coiled coils: A hypothesis. Biophys J 78(2):886-900.
12. Bentz J, Mittal A (2003) Architecture of the influenza hemagglutinin membrane fusion site. Biochim Biophys Acta 1614(1):24-35. (Pubitemid 36851601)
13. Madhusoodanan M, Lazaridis T (2003) Investigation of pathways for the low-pH conformational transition in influenza hemagglutinin. Biophys J 84(3):1926-1939. (Pubitemid 36322955)
14. Onuchic JN, Wolynes PG (2004) Theory of protein folding. Curr Opin Struct Biol 14(1):70-75. (Pubitemid 38249595)
15. Bryngelson JD, Wolynes PG (1987) Spin-glasses and the statistical-mechanics of protein folding. Proc Natl Acad Sci USA 84(21):7524-7528.
16. Leopold PE, Montal M, Onuchic JN (1992) Protein folding funnels: A kinetic approach to the sequence-structure relationship. Proc Natl Acad Sci USA 89(18):8721-8725.
17. Whitford PC, et al. (2009) An all-atom structure-based potential for proteins: Bridging minimal models with all-atom empirical forcefields. Proteins 75(2):430-441.
18. Noel JK, Whitford PC, Sanbonmatsu KY, Onuchic JN (2010) SMOG@ctbp: Simplified deployment of structure-based models in GROMACS. Nucleic Acids Res 38(Web Server issue):W657-W661.
19. Noel JK, et al. (2012) Mirror images as naturally competing conformations in protein folding. J Phys Chem B 116(23):6880-6888.
20. Lammert H, Schug A, Onuchic JN (2009) Robustness and generalization of structure-based models for protein folding and function. Proteins 77(4):881-891.
21. Carr CM, Kim PS (1993) A spring-loaded mechanism for the conformational change of influenza hemagglutinin. Cell 73(4):823-832. (Pubitemid 23159019)
22. Chen J, Skehel JJ, Wiley DC (1999) N- and C-terminal residues combine in the fusion-pH influenza hemagglutinin HA(2) subunit to form an N cap that terminates the triple-stranded coiled coil. Proc Natl Acad Sci USA 96(16):8967-8972. (Pubitemid 29374691)
23. Cho SS, Levy Y, Wolynes PG (2006) P versus Q: Structural reaction coordinates capture protein folding on smooth landscapes. Proc Natl Acad Sci USA 103(3):586-591. (Pubitemid 43153069)
24. Best RB, Hummer G, Eaton WA (2013) Native contacts determine protein folding mechanisms in atomistic simulations. Proc Natl Acad Sci USA 110(44):17874-17879.
25. Isin B, Doruker P, Bahar I (2002) Functional motions of influenza virus hemagglutinin: A structure-based analytical approach. Biophys J 82(2):569-581. (Pubitemid 34111201)
26. Okazaki K, Koga N, Takada S, Onuchic JN, Wolynes PG (2006) Multiple-basin energy landscapes for large-amplitude conformational motions of proteins: Structure-based molecular dynamics simulations. Proc Natl Acad Sci USA 103(32):11844-11849. (Pubitemid 44215774)
27. Miyashita O, Onuchic JN, Wolynes PG (2003) Nonlinear elasticity, proteinquakes, and the energy landscapes of functional transitions in proteins. Proc Natl Acad Sci USA 100(22):12570-12575. (Pubitemid 37339939)
28. Whitford PC, Sanbonmatsu KY, Onuchic JN (2012) Biomolecular dynamics: Order-disorder transitions and energy landscapes. Rep Prog Phys 75(7):076601.
29. Buchan DWA, Minneci F, Nugent TCO, Bryson K, Jones DT (2013) Scalable web services for the psipred protein analysis workbench. Nucleic Acids Res 41(Web Server issue):W349-W357.
30. Gething MJ, Doms RW, York D, White J (1986) Studies on the mechanism of membrane fusion: Site-specific mutagenesis of the hemagglutinin of influenza virus. J Cell Biol 102(1):11-23. (Pubitemid 16155549)
31. Godley L, et al. (1992) Introduction of intersubunit disulfide bonds in the membrane-distal region of the influenza hemagglutinin abolishes membrane fusion activity. Cell 68(4):635-645.
32. Weissenhorn W, Dessen A, Harrison SC, Skehel JJ, Wiley DC (1997) Atomic structure of the ectodomain from HIV-1 gp41. Nature 387(6631):426-430. (Pubitemid 27227210)
33. Weber T, et al. (1994) Evidence for H(+)-induced insertion of influenza hemagglutinin HA2 N-terminal segment into viral membrane. J Biol Chem 269(28):18353-18358.
34. Wharton SA, et al. (1995) Electron microscopy of antibody complexes of influenza virus haemagglutinin in the fusion pH conformation. EMBO J 14(2):240-246.
35. White JM, Delos SE, Brecher M, Schornberg K (2008) Structures and mechanisms of viral membrane fusion proteins: Multiple variations on a common theme. Crit Rev Biochem Mol Biol 43(3):189-219. (Pubitemid 351883153)
36. Singh JP, Whitford PC, Hayre NR, Onuchic J, Cox DL (2012) Massive conformation change in the prion protein: Using dual-basin structure-based models to find misfolding pathways. Proteins 80(5):1299-1307.
37. Lu Q, Wang J (2008) Single molecule conformational dynamics of adenylate kinase: Energy landscape, structural correlations, and transition state ensembles. J Am Chem Soc 130(14):4772-4783. (Pubitemid 351500112)
38. Noel JK, Whitford PC, Onuchic JN (2012) The shadow map: A general contact definition for capturing the dynamics of biomolecular folding and function. J Phys Chem B 116(29):8692-8702.
39. Chen J, et al. (1995) A soluble domain of the membrane-anchoring chain of influenza virus hemagglutinin (HA2) folds in Escherichia coli into the low-pH-induced conformation. Proc Natl Acad Sci USA 92(26):12205-12209. (Pubitemid 26014039)
40. Lu Y, Welsh JP, Swartz JR (2014) Production and stabilization of the trimeric influenza hemagglutinin stem domain for potentially broadly protective influenza vaccines. Proc Natl Acad Sci USA 111(1):125-130.