Sequential activation of the three protomers in the Moloney murine leukemia virus Env

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

Volumn 114, Issue 10, 2017, Pages 2723-2728

  Sjöberg, Mathilda ^a   Löving, Robin ^a,b   Lindqvist, Birgitta ^a   Garoff, Henrik ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

BN PAGE; Disulfide isomerase; Intermediate; Viral membrane fusion

Indexed keywords

DISULFIDE; OLIGOMER; THIOL; VIRUS ENVELOPE PROTEIN; VIRUS FUSION PROTEIN;

ALKYLATION; ANIMAL CELL; ARTICLE; CALCIUM DEPLETION; DENSITY GRADIENT CENTRIFUGATION; DISSOCIATION; IN VITRO STUDY; ISOMERIZATION; MOLONEY MURINE LEUKEMIA VIRUS; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; RAT; ULTRACENTRIFUGATION; ANIMAL; CELL LINE; CHEMISTRY; GENETICS; ISOMERISM; MOUSE; PATHOGENICITY; PROTEIN SUBUNIT; SURFACE PROPERTY; VIRUS ENTRY;

ALKYLATION; ANIMALS; CELL LINE; DISULFIDES; ISOMERISM; MICE; MOLONEY MURINE LEUKEMIA VIRUS; PROTEIN SUBUNITS; RATS; SURFACE PROPERTIES; VIRAL ENVELOPE PROTEINS; VIRAL FUSION PROTEINS; VIRUS INTERNALIZATION;

EID: 85014722231     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1617264114     Document Type: Article

References (34)

1. 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.
2. Bullough PA, Hughson FM, Skehel JJ, Wiley DC (1994) Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 371(6492):37-43.
3. Pancera M, et al. (2014) Structure and immune recognition of trimeric pre-fusion HIV-1 Env. Nature 514(7523):455-461.
4. 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.
5. McLellan JS, et al. (2013) Structure of RSV fusion glycoprotein trimer bound to a prefusion-specific neutralizing antibody. Science 340(6136):1113-1117.
6. McLellan JS, Yang Y, Graham BS, Kwong PD (2011) Structure of respiratory syncytial virus fusion glycoprotein in the postfusion conformation reveals preservation of neutralizing epitopes. J Virol 85(15):7788-7796.
7. Yin HS, Wen X, Paterson RG, Lamb RA, Jardetzky TS (2006) Structure of the para-influenza virus 5 F protein in its metastable, prefusion conformation. Nature 439(7072):38-44.
8. Yin HS, Paterson RG, Wen X, Lamb RA, Jardetzky TS (2005) Structure of the uncleaved ectodomain of the paramyxovirus (hPIV3) fusion protein. Proc Natl Acad Sci USA 102(26):9288-9293.
9. Weissenhorn W, Carfí A, Lee KH, Skehel JJ, Wiley DC (1998) Crystal structure of the Ebola virus membrane fusion subunit, GP2, from the envelope glycoprotein ectodomain. Mol Cell 2(5):605-616.
10. Lee JE, et al. (2008) Structure of the Ebola virus glycoprotein bound to an antibody from a human survivor. Nature 454(7201):177-182.
11. Walls AC, et al. (2016) Cryo-electron microscopy structure of a coronavirus spike glycoprotein trimer. Nature 531(7592):114-117.
12. Supekar VM, et al. (2004) Structure of a proteolytically resistant core from the severe acute respiratory syndrome coronavirus S2 fusion protein. Proc Natl Acad Sci USA 101(52):17958-17963.
13. 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.
14. Albritton LM, Tseng L, Scadden D, Cunningham JM (1989) A putative murine ecotropic retrovirus receptor gene encodes a multiple membrane-spanning protein and confers susceptibility to virus infection. Cell 57(4):659-666.
15. Wang H, Kavanaugh MP, North RA, Kabat D (1991) Cell-surface receptor for ecotropic murine retroviruses is a basic amino-acid transporter. Nature 352(6337):729-731.
16. Davey RA, Hamson CA, Healey JJ, Cunningham JM (1997) In vitro binding of purified murine ecotropic retrovirus envelope surface protein to its receptor, MCAT-1. J Virol 71(11):8096-8102.
17. Lavillette D, Boson B, Russell SJ, Cosset FL (2001) Activation of membrane fusion by murine leukemia viruses is controlled in cis or in trans by interactions between the receptor-binding domain and a conserved disulfide loop of the carboxy terminus of the surface glycoprotein. J Virol 75(8):3685-3695.
18. Barnett AL, Davey RA, Cunningham JM (2001) Modular organization of the Friend murine leukemia virus envelope protein underlies the mechanism of infection. Proc Natl Acad Sci USA 98(7):4113-4118.
19. Opstelten DJ, Wallin M, Garoff H (1998) Moloney murine leukemia virus envelope protein subunits, gp70 and Pr15E, form a stable disulfide-linked complex. J Virol 72(8):6537-6545.
20. Pinter A, Kopelman R, Li Z, Kayman SC, Sanders DA (1997) Localization of the labile disulfide bond between SU and TM of the murine leukemia virus envelope protein complex to a highly conserved CWLC motif in SU that resembles the active-site sequence of thiol-disulfide exchange enzymes. J Virol 71(10):8073-8077.
21. Wallin M, Ekström M, Garoff H (2004) Isomerization of the intersubunit disulphide-bond in Env controls retrovirus fusion. EMBO J 23(1):54-65.
22. Wu SR, et al. (2008) Turning of the receptor-binding domains opens up the murine leukaemia virus Env for membrane fusion. EMBO J 27(20):2799-2808.
23. Fass D, Harrison SC, Kim PS (1996) Retrovirus envelope domain at 1.7 angstrom resolution. Nat Struct Biol 3(5):465-469.
24. Bartesaghi A, Merk A, Borgnia MJ, Milne JL, Subramaniam S (2013) Prefusion structure of trimeric HIV-1 envelope glycoprotein determined by cryo-electron microscopy. Nat Struct Mol Biol 20(12):1352-1357.
25. Sjöberg M, Lindqvist B, Garoff H (2008) Stabilization of TM trimer interactions during activation of moloney murine leukemia virus Env. J Virol 82(5):2358-2366.
26. Leikina E, Ramos C, Markovic I, Zimmerberg J, Chernomordik LV (2002) Reversible stages of the low-pH-triggered conformational change in influenza virus hemagglutinin. EMBO J 21(21):5701-5710.
27. Munro JB, et al. (2014) Conformational dynamics of single HIV-1 envelope trimers on the surface of native virions. Science 346(6210):759-763.
28. Jiao J, Rebane AA, Ma L, Gao Y, Zhang Y (2015) Kinetically coupled folding of a single HIV-1 glycoprotein 41 complex in viral membrane fusion and inhibition. Proc Natl Acad Sci USA 112(22):E2855-E2864.
29. Lin X, et al. (2014) Order and disorder control the functional rearrangement of influenza hemagglutinin. Proc Natl Acad Sci USA 111(33):12049-12054.
30. Löving R, Sjöberg M, Wu S-R, Binley JM, Garoff H (2013) Inhibition of the HIV-1 spike by single-PG9/16-antibody binding suggests a coordinated-activation model for its three protomeric units. J Virol 87(12):7000-7007.
31. Colicelli J, Goff SP (1988) Sequence and spacing requirements of a retrovirus integration site. J Mol Biol 199(1):47-59.
32. Löving R, Kronqvist M, Sjöberg M, Garoff H (2011) Cooperative cleavage of the R peptide in the Env trimer of Moloney murine leukemia virus facilitates its maturation for fusion competence. J Virol 85(7):3262-3269.
33. Li K, et al. (2007) The conserved His8 of the Moloney murine leukemia virus Env SU subunit directs the activity of the SU-TM disulphide bond isomerase. Virology 361(1):149-160.
34. Rein A, Mirro J, Haynes JG, Ernst SM, Nagashima K (1994) Function of the cytoplasmic domain of a retroviral transmembrane protein: p15E-p2E cleavage activates the membrane fusion capability of the murine leukemia virus Env protein. J Virol 68(3):1773-1781.