Structure of a murine leukemia virus receptor-binding glycoprotein 2.0 angstrom resolution

Science

Volumn 277, Issue 5332, 1997, Pages 1662-1666

  Fass, Deborah ^a   Davey, Robert A ^a   Hamson, Christian A ^a   Kim, Peter S ^a   Cunningham, James M ^a   Berger, James M ^a  

^a NONE

Author keywords

[No Author keywords available]

Indexed keywords

RECEPTOR PROTEIN; VIRUS ENVELOPE PROTEIN; VIRUS RECEPTOR;

ARTICLE; FRIEND LEUKEMIA VIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; RETROVIRUS INFECTION; VIRUS CELL INTERACTION; VIRUS ENVELOPE; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; CARRIER PROTEINS; CRYSTALLOGRAPHY, X-RAY; FRIEND MURINE LEUKEMIA VIRUS; GLYCOPROTEINS; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; RECEPTORS, VIRUS; VIRAL ENVELOPE PROTEINS;

FRIEND MURINE LEUKEMIA VIRUS; MAMMALIA; MURINAE; MURINE LEUKEMIA VIRUS; UNIDENTIFIED RETROVIRUS;

EID: 0030820095     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.277.5332.1662     Document Type: Article

References (46)

1. E. Hunter and R. Swanstrom, Curr. Top. Microbiol. Immunol. 157, 187 (1990).
2. A. E. Smith, Annu. Rev. Microbiol. 49, 807 (1995).
3. MLVS have been grouped on the basis of superinfectivity resistance, the phenomenon whereby cells preinfected with an MLV cannot be infected by an exogenous virus that presumably utilizes the same receptor. These groups have been named according to their host ranges: ecotropic, amphotropic, polytropic, and xenotropic. Fr-MLV is an ecotropic MLV and infects only murine and certain other rodent cells. Amphotropic and polytropic viruses infect both murine and nonmurine cells, whereas xenotropic viruses infect only nonmurine cells.
4. L. M. Albritton, L. Tseng, D. Scadden, J. M. Cunningham, Cell 57, 659 (1989); J. W. Kim, E. I. Closs, L. M. Albritton, J. M. Cunningham, Nature 352, 725 (1991); H. Wang, M. P. Kavanaugh, R. A. North, D. Kabat, ibid., p. 729.
5. L. M. Albritton, L. Tseng, D. Scadden, J. M. Cunningham, Cell 57, 659 (1989); J. W. Kim, E. I. Closs, L. M. Albritton, J. M. Cunningham, Nature 352, 725 (1991); H. Wang, M. P. Kavanaugh, R. A. North, D. Kabat, ibid., p. 729.
6. L. M. Albritton, L. Tseng, D. Scadden, J. M. Cunningham, Cell 57, 659 (1989); J. W. Kim, E. I. Closs, L. M. Albritton, J. M. Cunningham, Nature 352, 725 (1991); H. Wang, M. P. Kavanaugh, R. A. North, D. Kabat, ibid., p. 729.
7. 2-terminal domain of SU expressed in isolation is sufficient to mediate superinfectivity resistance in both ecotropic and amphotropic MLVs (21). Furthermore, this domain binds MCAT-1 in vitro (6).
8. R. A. Davey, C. A. Hamson, J. M. Cunningham, J. Virol., in press.
9. A. Pinter, W. J. Honnen, J.-S. Tung, P. V. O'Donnell, U. Hammerting, Virology 116, 499 (1982).
10. 86 of another. Data to 2.8 Å were subsequently collected on a crystal grown in calcium acetate. The lengths of unit cell edges b and c were decreased in these crystals by 2.8 and 3.9%, respectively (a = 55.3 Å, b = 66.5 Å, C = 77.3 Å, α = β = γ = 90°). Molecular replacement with the program Amore (25) and refinement to a free R factor of 29.4% demonstrated that the packing is shifted slightly but significantly in these crystals, diminishing the distance between symmetry-related molecules and eliminating the intersubunit zinc ion-binding sites. Therefore, the zinc ion-binding sites are not integral to the Fr-RBD structure. There are no significant differences between the protein structures refined against data from the zinc-or calcium-containing crystals.
11. Although strand 3 contains two prolines that prohibit it from being considered a β strand according to standard secondary structure classification schemes such as that of Kabsch and Sander (26), we consider it a β strand here because it is in a position to make four backbone hydrogen bonds to strand 7.
12. M. Under, D. Under, J. Hahnen, H.-H. Schott, S. Stirm, Eur. J. Biochem. 203, 65 (1992). Four disulfide bonds (cysteines 46 and 98, 72 and 87, 73 and 83, and 178 and 184) are in the helical lobe, whereas two disulfide bonds (cysteines 121 to 141 and 133 to 146) are in a loop between strands 4 and 5. Only one cysteine, at position 121, lies in a β strand.
13. L. Holm and C. Sander, J. Mol. Biol. 233, 123 (1993); Nucleic Acids Res. 24, 206 (1996). The 3D-ali server, a network service for comparing protein structures in three dimensions, is available at www.embl-heidelberg.de/argos/ali/al.html.
14. L. Holm and C. Sander, J. Mol. Biol. 233, 123 (1993); Nucleic Acids Res. 24, 206 (1996). The 3D-ali server, a network service for comparing protein structures in three dimensions, is available at www.embl-heidelberg.de/argos/ali/al.html.
15. The following proteins gave z scores ranging from 3.4 to 2.0 and α-carbon root mean square deviations (RMSDs) between 3.1 and 4.9 Å over about 90 residues each (an alignment was found for strands 3 through 9, but the helical lobe and strands 1 and 2 could not be aligned): single-chain FV fragment, light chain (pdb1mfa.ent); human CD2 (pdb1hnf.ent); OPG2 Fab fragment, heavy chain (pdb1opg.ent); rat CD4, domain 3 (pdb1cid.ent); human CD8, domain 1 (pdb1cd8.ent); Fab fragment, light chain (pdb1mlb.ent); beta chain of murine T cell antigen receptor, variable domain (pdb1bec.ent); human CD4, domain 1 (pdb3cd4.ent); human coagulation factor XIII (pdb1ggt.ent); E coli PAP*D chaperone (pdb3dpa.ent); human p53 tumor suppressor protein (pdb1tup.ent); human VCAM-1, domain 1 (pdb1vca.ent); and murine N-cadherin, domain 1 (pdb1nci.ent).
16. These variable regions have previously been referred to as VRA and VRB (27). Biased by the Fr-RBD structure and given the existence of a conserved region near the end of VRA, we divided VRA into two distinct variable regions, one that we still refer to as VRA and the other that we now call VRC.
17. D. Ott and A. Rein, J. Virol. 66, 4632 (1992).
18. C. Peredo, L. O'Reilly, K. Gray, M. J. Roth, ibid. 70, 3142 (1996); R. A. Morgan et al., ibid. 67, 4712 (1993).
19. C. Peredo, L. O'Reilly, K. Gray, M. J. Roth, ibid. 70, 3142 (1996); R. A. Morgan et al., ibid. 67, 4712 (1993).
20. We generated a packing model for Fr-RBD as it would exist in the trimeric envelope glycoprotein complex. We constructed this trimer packing model manually by placing the carbohydrates (10) toward solvent, keeping variable sequences surface-exposed rather than at trimer contacts and maximizing the contact area while avoiding steric clashes. Although VRC is distant from VRA and VRB within an Fr-RBD monomer, VRC from one subunit is close to VRB of the adjacent subunit of the trimer model, such that there are only three variable lobes per trimer, with each being composed of sequences from two Fr-RBD subunits (D. Fass, thesis, Massachusetts Institute of Technology, Cambridge, 1997).
21. A. J. MacKrell, N. W. Soong, C. M. Curtis, W. F. Anderson, J. Virol. 70, 1768 (1996).
22. 126, is partially buried and in position to form a hydrogen bond to the backbone carbonyl of residue 134. This interaction could anchor the VRC loop or aid in proper disulfide bond formation of nearby cysteines and is apparently also critical for proper folding and processing.
23. S. Valsesia-Whittman et al., J. Virol. 70, 2059 (1996).
24. N. Kasahara, A. M. Dozy, Y. W. Kan, Science 266, 1373 (1994).
25. J. M. Heard and O. Danos, J. Virol. 65, 4026 (1991); J.-L. Battini, O. Danos, J. M. Heard, ibid. 69, 713 (1995).
26. J. M. Heard and O. Danos, J. Virol. 65, 4026 (1991); J.-L. Battini, O. Danos, J. M. Heard, ibid. 69, 713 (1995).
27. C. Friend, J. Exp. Med. 105, 307 (1957); W. Koch, G. Hunsmann, R. Friedrich, J. Virol. 45, 1 (1983).
28. C. Friend, J. Exp. Med. 105, 307 (1957); W. Koch, G. Hunsmann, R. Friedrich, J. Virol. 45, 1 (1983).
29. Single-letter abbreviations for the amino acid residues are as follows: A, Ala; D, Asp; E, Glu; G, Gly; I, Ile; P, Pro; R, Arg; V, Val; and Y, Tyr.
30. D. J. Goldstein and R. Schlegel, EMBO J. 9, 137 (1990).
31. J. Navaza, Acta Crystallogr. Sect. A Found. Crystallogr. 50, 157 (1994).
32. W. Kabsch and C. Sander, Biopolymers 22, 2577 (1983).
33. J.-L. Battini, J. M. Heard, O. Danos, J. Virol. 66, 1468 (1992).
34. Z. Otwinowski, in Data Collection and Processing, L. Sawyer, N. Isaacs, S. Bailey, Eds. [Science and Engineering Research Council (SERC), Daresbury Laboratory, Warrington, UK, 1993], pp. 56-62.
35. Collaborative Computational Project, Number 4, Acta Crystallogr. Sect. D Biol. Crystallogr. 50, 760 (1994).
36. Z. Otwinowski, in Isomorphous Replacement and Anomalous Scattering, W. Wolf, P. R. Evans, A. G. W. Leslie, Eds. (SERC Daresbury Laboratory, Warrington, UK, 1991), pp. 80-86.
37. K. Cowtan, Joint CCP4 ESF-EACBM Newsl. Protein Crystallogr. 31, 34 (1994).
38. T, A. Jones and M. Kjeldgaard, O - The Manual [online], Uppsala, Sweden, 1992. Available at www. imsb.au.dk/∼mok/o.
39. A. T. Brünger, X-PLOR Version 3.1. A System for X-ray Crystallography and NMR ( Yale Univ. Press, New Haven, CT, 1992).
40. 3/M, Nature 355, 472 (1992).
41. K. Y. Zhang and D. Eisenberg, Protein Sci. 3, 687 (1994).
42. M. Carson, J. Appl. Crystallogr. 24, 958 (1991).
43. P. Kraulis, ibid., p. 924.
44. P. Bork, L. Holm, C. Sander, J. Mol. Biol. 242, 309 (1994).
45. A. Nicholls, K. A. Sharp, B. Honig, Proteins 11, 281, 1991.
46. We thank S. C. Harrison, S. J. Gamblin, and D. C. Wiley for helpful discussions and N. Azubuine for media preparation. J.M.B. is a Whitehead Fellow and acknowledges support from the W. M. Keck Foundation. This work was funded by the Howard Hughes Medical Institute and utilized the W. M. Keck Foundation X-ray Crystallography Facility at the Whitehead Institute. The coordinates have been deposited in the Protein Data Bank with accession number 1AOL