Maturation cleavage of the murine leukemia virus Env precursor separates the transmembrane subunits to prime it for receptor triggering

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

Volumn 109, Issue 20, 2012, Pages 7735-7740

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

^a KAROLINSKA INSTITUTE   (Sweden)

^b NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

Author keywords

Retrovirus; Spike protein; Three dimensional structure

Indexed keywords

AMPRENAVIR; MEMBRANE PROTEIN; MUTANT PROTEIN; TRITON X 100; VIRUS ENVELOPE PROTEIN;

ARTICLE; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; HUMAN; HUMAN CELL; MOLECULAR MODEL; MOLONEY LEUKEMIA ONCOVIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN INTERACTION; PROTEIN PROCESSING; PROTEIN STRUCTURE; PROTEIN SUBUNIT; SEDIMENTATION; SUCROSE GRADIENT;

CRYOELECTRON MICROSCOPY; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FRACTIONATION, FIELD FLOW; GENE PRODUCTS, ENV; LEUKEMIA VIRUS, MURINE; MODELS, MOLECULAR; MOLONEY MURINE LEUKEMIA VIRUS; OCTOXYNOL; PROTEIN CONFORMATION; PROTEIN PRECURSORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN SUBUNITS;

MOLONEY MURINE LEUKEMIA VIRUS; MURINE LEUKEMIA VIRUS;

EID: 84861218412     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1118125109     Document Type: Article

References (30)

1. Hallenberger S, et al. (1992) Inhibition of furin-mediated cleavage activation of HIV-1 glycoprotein gp160. Nature 360:358-361. (Pubitemid 23000676)
2. Green N, et al. (1981) Sequence-specific antibodies show that maturation of Moloney leukemia virus envelope polyprotein involves removal of a COOH-terminal peptide. Proc Natl Acad Sci USA 78:6023-6027. (Pubitemid 12247457)
3. Schultz A, Rein A (1985) Maturation of murine leukemia virus env proteins in the absence of other viral proteins. Virology 145:335-339. (Pubitemid 15016456)
4. Shapiro SZ, Strand M, August JT (1976) High molecular weight precursor polypeptides to structural proteins of Rauscher murine leukemia virus. J Mol Biol 107:459-477.
5. Ng VL, Wood TG, Arlinghaus RB (1982) Processing of the env gene products of Moloney murine leukaemia virus. J Gen Virol 59:329-343. (Pubitemid 12094616)
6. Hunter E (1997) Viral entry and receptors. Retroviruses, eds Coffin JM, Hughes SH, Varmus HE (Cold Spring Harbor Lab Press, Cold Spring Harbor, NY), pp 71-119.
7. Henderson LE, Sowder R, Copeland TD, Smythers G, Oroszlan S (1984) Quantitative separation of murine leukemia virus proteins by reversed-phase high-pressure liquid chromatography reveals newly described gag and env cleavage products. J Virol 52:492-500. (Pubitemid 15202485)
8. Ragheb JA, Anderson WF (1994) pH-independent murine leukemia virus ecotropic envelope-mediated cell fusion: Implications for the role of the R peptide and p12E TM in viral entry. J Virol 68:3220-3231. (Pubitemid 24129772)
9. 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 68:1773-1781. (Pubitemid 24065746)
10. Förster F, Medalia O, Zauberman N, Baumeister W, Fass D (2005) Retrovirus envelope protein complex structure in situ studied by cryo-electron tomography. Proc Natl Acad Sci USA 102:4729-4734. (Pubitemid 40471522)
11. Wu SR, et al. (2008) Turning of the receptor-binding domains opens up the murine leukaemia virus Env for membrane fusion. EMBO J 27:2799-2808.
12. Pinter A, Honnen WJ, Tung JS, O'Donnell PV, Hämmerling U (1982) Structural domains of endogenous murine leukemia virus gp70s containing specific antigenic determinants defined by monoclonal antibodies. Virology 116:499-516. (Pubitemid 12163303)
13. Fass D, et al. (1997) Structure of a murine leukemia virus receptor-binding glycoprotein at 2.0 angstrom resolution. Science 277:1662-1666. (Pubitemid 27446228)
14. 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 75:3685-3695. (Pubitemid 32246378)
15. 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 98:4113-4118. (Pubitemid 32249907)
16. Wallin M, Ekstrom M, Garoff H (2004) Isomerization of the intersubunit disulphide-bond in Env controls retrovirus fusion. EMBO J 23:54-65. (Pubitemid 38165747)
17. Löving R, Li K, Wallin M, Sjöberg M, Garoff H (2008) R-peptide cleavage potentiates fusion-controlling isomerization of the intersubunit disulfide in Moloney murine leukemia virus Env. J Virol 82:2594-2597. (Pubitemid 351293563)
18. Taylor GM, Sanders DA (2003) Structural criteria for regulation of membrane fusion and virion incorporation by the murine leukemia virus TM cytoplasmic domain. Virology 312:295-305. (Pubitemid 36960006)
19. Yang C, Compans RW (1997) Analysis of the murine leukemia virus R peptide: Delineation of the molecular determinants which are important for its fusion inhibition activity. J Virol 71:8490-8496. (Pubitemid 27446430)
20. Aguilar HC, Anderson WF, Cannon PM (2003) Cytoplasmic tail of Moloney murine leukemia virus envelope protein influences the conformation of the extracellular domain: Implications for mechanism of action of the R peptide. J Virol 77:1281-1291. (Pubitemid 36055551)
21. 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 85:3262-3269.
22. Zavorotinskaya T, Albritton LM (1999) A hydrophobic patch in ecotropic murine leukemia virus envelope protein is the putative binding site for a critical tyrosine residue on the cellular receptor. J Virol 73:10164-10172.
23. Fass D, Harrison SC, Kim PS (1996) Retrovirus envelope domain at 1.7 angstrom resolution. Nat Struct Biol 3:465-469.
24. Waning DL, Russell CJ, Jardetzky TS, Lamb RA (2004) Activation of a paramyxovirus fusion protein is modulated by inside-out signaling from the cytoplasmic tail. Proc Natl Acad Sci USA 101:9217-9222. (Pubitemid 38812855)
25. Sjöberg M, Wallin M, Lindqvist B, Garoff H (2006) Furin cleavage potentiates the membrane fusion-controlling intersubunit disulfide bond isomerization activity of leukemia virus Env. J Virol 80:5540-5551.
26. Colicelli J, Goff SP (1988) Sequence and spacing requirements of a retrovirus integration site. J Mol Biol 199(1):47-59.
27. 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 72:6537-6545. (Pubitemid 28323968)
28. Schägger H, von Jagow G (1991) Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal Biochem 199:223-231.
29. Sjöberg M, Lindqvist B, Garoff H (2008) Stabilization of TM trimer interactions during activation of Moloney murine leukemia virus Env. J Virol 82:2358-2366. (Pubitemid 351293536)
30. Wu SR, et al. (2010) Single-particle cryoelectron microscopy analysis reveals the HIV-1 spike as a tripod structure. Proc Natl Acad Sci USA 107:18844-18849.